Health Benefits of Starch

Abstract

In recent years, scientific research has focused on evaluating the relationship between consumption and the effect of food components on the body, with the aim of improving the health condition of the population. In particular, starch is the main component in grains and provides most of the energy in the diet. It is classified according to its nutritional characteristics as rapidly digestible starch (RDS), slowly digestible starch (SDS), and non-digestible starch (RS). Several studies have reported that different starch fractions show a correlation between digestibility and assimilation with physiological effect and metabolic impact. Each type of starch fraction consumed shows a different postprandial response, such that SDS and RS generate a slower absorption rate and lower serum glucose concentration, leading to a gradual uptake of glucose into the tissue, as well as a probiotic effect. Current reports suggest that consumption of SDS- and RS-rich products can generate a postprandial response of prolonged glucose uptake without hyperglycemic peaks, and improve the efficiency of modulation of carbohydrate metabolism. In this regard, there is a growing interest in carbohydrates with functional effects generating an emerging area of study. The aim of this chapter is to describe the potential functional effect and metabolic impact of consumption of the SDS and SR fractions of starch.

1. Introduction

Several research has been focused on investigating the relation between the intake of the different compounds existing in food and their health benefits [1]. A special emphasis has been paid to study their potential benefit effects on chronic and metabolic diseases, such as diabetes or obesity, in order to improve the life quality of the individuals with these pathologies [2, 3]. In this context, carbohydrates (CH) are the main macronutrient in food and contribute 45–55% of the required energy [4]. Specifically, starch is the main CH of the diet, and therefore, it provides the majority of the required energy. Starch is content on cereals, legumes, roots, nuts, and their derived products. During gastrointestinal digestion, starch is first hydrolyzed in the mouth by the activity of the salivary α amylase, able to hydrolyze the glucose-glucose bonds with direction α(1-4), releasing diverse dextrins and maltose [5]. The starch digestion is completed in the intestine by the digestive action of the intestinal enzymes α amylase, isomaltase, and glucoamylase, that provoke the starch debranching on the α(1-6) bonds and the hydrolysis of the α(1-4) bonds, releasing high amounts of glucose [6, 7]. These glucose are absorbed in the intestine by the Sodium-Dependent Glucose Transporter 1 (SGLUT-1), causing a glycaemia increase that provokes the release of insulin [8, 9]. However, the various botanical and industrial starches show different behaviors during the gastrointestinal digestion process, as a consequence of their different structural characteristics and physicochemical properties [7]. Therefore, regarding their digestion behavior, the diverse starch fractions can be classified as rapidly digestible starch (RDS), slowly digestible starch (SDS) [7, 10] and a crystallized starch fraction non-digestible denominated resistant starch (RS) [11, 12, 13]. The botanical origin shows a great influence in starch digestibility since it set up their structural characteristics and physicochemical properties, and therefore, the amount of each starch fraction [5, 7, 10].

The consumption of food rich in SDS is associated with a progressive release of glucose, maintaining a sustained energy source along the time compared with products with low SDS amounts and higher RDS contents [6, 10, 12, 13]. As consequence, the metabolic response generated by foods with higher SDS content shows a clear association with better postprandial metabolic parameters in healthy people but also in diabetic and obese individuals [13, 14, 15, 16]. Thus, it is necessary to study and identify the mechanisms that relate the differences between the total glucose intake under starch form and the total absorber glucose after starch intake in order to understand the glycaemia response and metabolic profile of the different starches [14, 15]. The kinetic of the intestinal absorption of the released glucose can be used as valuable information to predict the postprandial changes in the blood glucose concentration and plasmatic insulin circulation [17, 18]. In this context, the diverse postprandial glycemic responses have been associated with the different starch fractions, where SDS and RS fractions show a slower glucose absorption rate, and therefore, attenuated glycemic response as well as less intense insulinemic responses [15, 19, 20]. Since high glycemic and insulinemic responses are associated with chronic diseases, mainly with the development of type 2 diabetes, a growing interest in the study of the CH and their metabolic responses exists, principally focused on the CH associated with a lower and maintained glucose absorption and therefore a mitigated glycemic response, characterized by the lack of hyperglycemic peaks and a maintained provided energy [19, 20].

2. Digestibility

Starch is largely digested among the gastrointestinal tract, being hydrolyses and absorbed at least 75% of the intake molecules [7, 21]. However, starch digestibility is conditioned by diverse factors, such as the acidity of the medium (a factor that reduces the activity of the amylase) or the cooking process, which gelatinize and solubilize the starch, increasing the accessibility of the digestive enzymes [4, 7, 9]. The starch digestion in the gastrointestinal tract occurs in diverse steps with the contribution of different digestive enzymes [8, 9, 16].

The first digestion step occurs in mouth digestion. Together with the reduction of the particle size of the intake of food by the chewing process, the release of salivary α amylase rules the digestion in the mouth. This enzyme shows a specific endo-hydrolytic activity on glucose-glucose α-(1,4) bonds but without activity on α-(1,6) bonds [10, 16, 22]. The endo-hydrolytic activity allows to hydrolyze the α-(1,4) bonds within the polymeric molecule, releasing lower glucose chains with direction α-(1,4), such as oligomers, maltotriose, or maltose [9, 18]. The mouth phase of the starch digestion is a short event because of the few time that takes the chewing and swallowing process, even though the first digestion products appears at 10–20 s after ingestion, increasing the digestion products as the mouth digestion progress. It is important to point that in contrast to other substrates, the starch size is higher than the digestive enzymes α-amylases, allowing many possible points within the molecule for the enzyme union, thus facilitating the enzyme activity [4, 9, 22].

The stomach digestion does not release specific enzymes with digestive action for the starch molecule. However, the swallowed saliva together with the alimentary bolus may exert a residual activity until reaching an acid pH able to inactivate the salivary α amylases. Consequently, the digestion of the complex CH can undergo total hydrolysis of 10–40% before reaching the small intestine [4, 22, 23]. During the intestinal digestion, starch is hydrolyzed by the activity of the intestinal α amylase, other endo-hydrolytic enzymes with activity on the glucose-glucose α-(1,4) bonds. However, this enzyme is not able to hydrolyze the α-(1,6) bonds existing in the branching amylopectin [10, 16, 18, 23]. Because of that, the activity of this enzyme is complemented with the activity of the isomaltase (able to hydrolyze the α-(1,6) bounds) and the glucoamylases, that hydrolyze α-(1,4) bounds mainly of glucose oligomers, such as dextrins. The combined action of these three enzymes becomes the successive digestion products, such as dextrins, oligosaccharides, and maltotriose, into maltose and glucose molecules. Besides, the action of the maltase enzyme of the intestine brush border becomes maltose into two glucose molecules [9, 16, 22]. The result of the complete digestion process of the ingested starch is a high amount of released glucose, being transported into the enterocytes by the transporter SGLUT-1 and excreted to the portal vein by the intestinal Glucose Transporter 2 (GLUT-2), provoking an increase of the glycaemia and an insulinemic response [14, 22, 23].

Starch digestibility is a factor of the food quality. The effect of the different starch fractions on the postprandial metabolism depends on the velocity and degree of the starch digestibility. SDS and SDS are categorized as glycemic starches and constitute the digestible starch fraction (DS). This DS fraction is hydrolyzed along the gastrointestinal tract whereas a fraction of the starch remains non-digestible, corresponding to the RS [4, 6, 7, 8]. The DS fraction is completely assimilated in the small intestine, responsible for the increase of the postprandial glycaemia [13, 14, 16, 24]. RS is characterized by a crystalline structure that avoids the digestibility of the molecule by the human digestive enzymes. As consequence, this fraction reaches the colonic tract, being fermented by the bacteria of the colonic microbiota, releasing short chain fatty acids (SCFA), such as butyric acid [11, 12, 25, 26]. The different digestibility found in the NS of the diverse botanical species has been explained as the interaction of various factors, such as the botanical source that condition the amount of each starch fraction, the starch granule size, the presence or absence of superficial pores on the starch granules, the relation amylose/amylopectin, the crystallinity degree on the molecule (correlated with the X-ray diffraction pattern) [24, 27], the association degree between diverse starch chains, the distribution and length of the branched chains of the amylopectin or the existence of interior channels and fractures on the starch molecule [24, 27, 28]. In addition, the industrial processing and cooking of starchy food can alter the starch properties, influencing the digestibility properties and also, the amount of each starch fraction [6, 7, 22, 29].

The rate and degree of starch amylolysis is determining factor in establishing the magnitude and duration of the postprandial glycaemic response. Currently, different in vitro tests have been considered to evaluate the rate and degree of starch hydrolysis as predictors of the physiological effect of food consumption [8, 17, 18, 23]. However, establishing the comparison of digestibility values found in the literature is a complicated task due to the variability in the methodology [8, 23, 27, 28, 30], as well as the variability of the type of enzyme used for the starch hydrolysis [16, 17, 28, 30]. In this context, the susceptibility level of the hydrolysis of retrograde samples depends on the type of α-amylase used (bacterial, fungal, pancreatic), enzyme concentration, hydrolysis time, and purity of the enzyme [17, 18, 28, 30, 31].

Among the aspects to consider studying and interpreting the in vitro digestibility of starch, and thus being able to establish postprandial physiological predictions, the understanding of the mechanics of action of digestive enzymes on starch hydrolysis should be studied. Currently, a kinetic model has been established that follows a pseudo-first order reaction for the analysis of starch hydrolysis, using as a tool the graph from the “logarithm-of-slope” (LOS) plot [17, 18]. This model allows conducting an analysis to be performed to classify the RDS, SDS, and RS fractions based on kinetic behavior in terms of a rate constant and the degree of hydrolysis. The in vitro hydrolysis level of starch is a frequently used indicator to determine the degree of total digestibility in starch samples. This parameter is represented by the equilibrium concentration (C∞) at the end time of the kinetics of amylolysis, represented by the digestograms [16, 17, 18, 23]. Digestion rates are measured by the kinetic rate constant (k) (pseudo-1st order rate constants for starch amylolysis).

The kinetic constants of amylolysis in native starches (NS) and gelatinized, as in the case of cereals such as corn and legumes such as beans and broad beans, present a similar degree of level of enzymatic activity and affinity of the enzyme for the substrate [32]. In general, the gelatinized NS LOS plots of corn, beans, and broad beans show similar kinetic behavior. This implies that in the fastest phase the easily accessible starch is hydrolyzed, presenting a relative duration of 30 min, and later it simultaneously passes to a slower phase, which shows that the behavior of the graphics tends to be of a single phase. This implies that the easily accessible fraction is more available to the action of α-amylase, resulting in an increase in the degree of digestibility expressed as C∞. The LOS graphs show a single linear phase hydrolysis process, considering a constant k with a similar behavior between the different varieties obtained by this method. Hydrolysis of gelatinized starches generally occurs in a single phase as gelatinization makes the starch fully accessible to the enzyme [33].

In the case of RS obtained by debranching and subsequent retrogradation of corn, beans, and broad beans, the LOS graphs show the behavior of an initial fast phase that inevitably has a prolongation. This implies that the reaction is characterized by a slower phase, and represents the fraction of starchless available, which is reflected in the values of k and C∞ [32]. Thus, the slopes of the LOS graphs of the RS are notably lower than the NS, consequently, lower values of k are obtained in the RS samples compared to the NS samples that reflect a slow phase of hydrolysis, showing a lower affinity of the enzyme for the substrate.

Studies in NS of these varieties have shown that hydrolysis is faster in the first phase because the enzyme more easily accesses the starch fractions of the amorphous regions [16, 18, 34]. Type A starch, which is characteristic of cereal starches, shows a high proportion of short chains in the cluster, due to a large number of branches, which are more widely dispersed within the cluster, increasing the number of access points for amylase and substrate [24, 35, 36]. In addition, it has been considered that the crystallinity pattern of starches conditions their digestibility. NS with type A crystallinity patterns have pores and channels, whereby the enzyme penetrates into them and the hydrolysis reaction starts from the hilum region towards the outside of the granules, thus favoring the degree and speed of starch hydrolysis [35, 36]. On the other hand, NS with a type B crystallinity pattern does not present pores, showing a non-porous surface, thus giving a different hydrolysis pattern than type A, because the enzymatic digestion starts from the starch surface. This promotes the degree and rate of hydrolysis to be lower [24, 33, 37]. Likewise, it has been observed that legume NS with a crystallinity pattern of type C (A + B) shows a lower degree of hydrolysis. It has been reported that the difference in the degree of amylolysis in starches with type C patterns, is influenced by the presence of fissures or cracks on the surface of the granule that some varieties of legumes present. These cracks would allow the enzymes to have a higher diffusivity and to penetrate more quickly into the granule, hydrolyzing more easily the starch chains close to the granule surface [34, 36, 37].

This phenomenon would explain the difference in RDS levels between the different legume varieties. Likewise, the levels of SDS and RS depend on the degree of structural organization of the double helices within the crystalline lamellae and the distribution of these lamellae in the granule [38, 39]. A starch with higher SDS and RS content is characterized by a decreased level of susceptibility to hydrolytic enzymes and consequently lower digestibility, generating a moderate postprandial response without hyperglycemic peaks [13, 19, 20, 40]. This type of starch is the most suitable for consumption in the diet, especially in diabetic situations [13, 14, 19, 20]. In the case of RS, they have a lower k constant compared to the digestion kinetics of NS and represent a decrease in the catalytic efficiency of α-amylase due to the high degree of crystallinity of RS [11, 12, 25]. A low value of k is estimated to reflect a lower diffusion and a slower phase in the hydrolysis process by α-amylase, due to the degree of crystallinity of the different fractions of RS which inhibits the action of α-amylase [16, 17, 18, 28].

3. Nutritional characteristics of the starch

Starch is constituted by two different CH polymers, amylose, and amylopectin. Amylose consists of linear chains of glucose molecules linked by α(1-4) bounds, whereas amylopectin is constituted by linear chains of glucose molecules linked by α(1-4) bounds, with branching points linked by α(1-4) bounds every 15–30 glucose molecules [24, 35, 36]. Regardless of the botanical origin of starch, it is always composed of these two polymers, changing their amylose/amylopectin ratio in relation to their botanical origin [24, 35, 36]. Therefore, the differences in the nutritional characteristics of the diverse starches are a consequence of their bioaccessibility and bioavailability that depends on their composition on RDS, SDS, and RS.

3.1 Factors that influence bioavailability

The starch digestibility is a consequence of intrinsic factors, such as the starch morphology and physicochemical properties, and of extrinsic factors, determined by the physiological conditions of the individuals [6, 7, 9, 28], with a variability regarding genetic factors [41].

The intrinsic factors are referred to the structural and physicochemical characteristics. These properties are related to the granule and highly influenced by the botanical origin [6, 7, 9], or are the result of applied processes during the industrial processing or cooking processes. These factors condition the ability and accessibility of the digestive enzymes to starch molecule, influencing the hydrolysis degree [41, 42], and therefore, the intrinsic properties condition the bioaccessibility and bioavailability degree of the molecule [40, 41, 42]. Since these factors directly modulate the digestibility, condition also postprandial response [39, 40, 41]. Diverse processes modify starch assimilation. The grinding of the grain provokes ruptures of the starch molecule, enhancing the efficiency of the gelatinization and allowing a greater interaction of the digestive enzymes, increasing the starch bioavailability. The food products elaborated with grinding grains are characterized by faster starch hydrolysis and an immediately postprandial response [6, 7, 9, 34, 40].

The extrinsic factors are referred to the physiological conditions of the individuals that determined the bioaccessibility and bioavailability of the starch. These factors include age, gender, metabolic conditions, pathological alterations of the digestive tract, the efficiency of the digestive process, gastrointestinal transit time, and genetic variations, among others [9, 22, 42]. Due to the genetic variation in the expression of the digestive enzymes [22, 41, 42] or because of specific physiological conditions, some individuals do not completely absorb the glucose release from the starch hydrolysis [6, 41, 42]. The food emptying from the stomach is a consequence of the gastric emptying, regulated by diverse factors such as the amount and volume of the ingested food, the type of macronutrient, the energy density of the intake, the particle size of the food matrix, the viscosity, the osmolality and the pH [7, 9]. Once the gastric content is released to the intestine, factors such as the viscosity influence the accessibility of the digestive enzymes to the chime and the nutrient releasing [9, 22]. In this context, the gastrointestinal transit time of the starch is inversely correlated with the amount of ingested starch and the contact time of the enzymes with the substrate [41, 42].

3.2 Classification of the diverse starch fractions

The digestibility and bioavailability of the starch vary depending on the intrinsic and extrinsic factors, closely related to the starch type and the botanical origin [6, 7, 9]. As consequence, starch can be classified according to their digestibility degree and releasing velocity of their constituent CH [6, 8, 10, 19, 21, 22, 43]. In this context, the diverse starch fractions can be classified according to these two parameters, the digestibility and assimilation degree, in three different fractions: rapid digestible starch (RDS), the slow digestive starch (SDS), and the resistant starch (RS) [6, 21, 28, 43]. All the starches are naturally constituted by an RSD and an SDS fraction, and a minor fraction of RS. The whole digestibility of the starch is a consequence of these three fractions and can be determined in vitro by measuring the glucose release of each fraction, as a predictor of their potential postprandial response [39, 40, 43].

The RDS is characterized to be the first completely digested fraction, showing a characteristic high velocity of glucose release, occurring the whole hydrolysis of this fraction within the first 20–30 min [6, 27, 28, 30]. The digestion of this fraction release oligosaccharide that are quickly hydrolyzed to glucose molecules [44]. This fraction is completely assimilated, being digested, and absorbed in the proximal duodenum [7, 24, 27, 28]. The behavior of this starch fraction during gastrointestinal digestion is a consequence of the amorphous structure of this starch fraction and the high gelatinization degree, being easily hydrolyzed by the digestive enzymes [6, 27, 28]. The RDS generate a fast increase of the glucose concentration in the blood after the starch intake and frequently provoke a hyperglycemic response. These highly fluctuant glucose levels generate increased stress on the regulatory systems of the glucose homeostasis with possible alterations or damages in cells, tissues, and organs [44]. Food with this characteristic (rich or enriched in RDS fraction) are the products with a high refinery degree, such as cereals flours used for bakery, pastries, biscuits, breath or fried foods, among others [24, 27, 29, 39].

Conversely, the SDS fraction is characterized by slow and progressive digestion, showing an intestinal absorption of the almost entire starch fraction. This starch fraction is composed of an amorphous but rigid structure, generating a more inaccessible structure that hinders the enzyme accessibility and an imperfect crystalline structure that limits the action of the digestive enzymes. As a consequence of this more complex accessibility for the digestive enzymes, the hydrolysis velocity is dramatically reduced, showing a slower digestion velocity [16, 39, 45]. The progressive release of glucose molecules resulting from its hydrolysis, allowing a progressive intestinal absorption of the glucose products, avoids high glycemic peaks, showing a lower but maintained postprandial response. This glycemic response is beneficial for healthy people but especially for diabetics [13, 14, 19, 30, 44]. The slow digestion and assimilation are related to several intrinsic factors of the starch molecule, as well as to structural changes that occurred during industrial processing or cooking [4, 6, 19, 27, 29, 44].

The structural properties of the food matrix may play an important role during starch digestion. When starch is contained internally in the food matrix, it plays an important role in reducing the velocity of the starch digestion because it get caught on the food matrix or by a barrier action of the rigid cell walls. This events are commons in legumes [7, 10, 27, 29, 45]. This coughed starch fraction is especially interesting for people with metabolic or chronic diseases, particularly type 2 diabetic or hyperlipidaemic ones [45].

RS is the starch fraction characterized by not be hydrolyzed by the digestible enzymes, reaching entirely the colonic tract [6, 11, 12, 21, 24, 25]. The European Research Project on Resistant Starch (EURESTA) defines RS as “the sum of starch and products of starch degradation not absorbed in the small intestine of healthy individuals” [11, 12]. When RS reaches the colonic tract, it is fermented into diverse SCFA, especially propionic and butyric acids, or conversely, it is eliminated through the fecal material [11, 12, 13, 25, 26]. Regarding their chemical nature, RS can be classified into diverse categories. Table 1 summarizes the diverse types of RS currently identified and their main characteristics. Some RS occurs naturally in food, existing in the starch granule, whereas others RS are the result of a structural reorganization on the molecule or the molecule interaction with other compounds, as a consequence of industrial processing, cooking, or intentioned chemical modifications [11, 12, 24, 25]. In any case, the RS formation is due to a structural reorganization of the amylose linear chains and their association with the amylopectin [25, 46, 47]. Accordingly, RS frequently occurs in starch molecules with a higher amylose/amylopectin ratio, increasing the available lineal chains of α-glucans to form crystalline and organized structures [24, 25, 46, 47, 48]. The molecular weight of these RS crystalline structures is close to 100 kDa.

Type	Source	Digestibility
AR-I.; Physically inaccessible starch, encapsulated into the morphological structures of the grains	Whole grains and/or partially grinded raw grains	Poor grade and velocity of assimilation
AR-II.; Granules of NS highly crystallized and non-gelatinized	Raw potatoes, bananas and legumes	Low digestibility and poor assimilation
AR-III.; Crystallized starch o retrograded	Bread and baked goods	Low digestibility and poor assimilation
AR-IV.; Modified starch with chemical processes (such as interlinking process or esterification)	Specific ingredients chemically developed	Resistant or partially digestible
AR-V.; Amylose-lipid complex (type V) as consequence of food processing	Bread and baked goods	Resistant to the digestion process

Table 1.

Classification of the diverse types of RS.

4. Functional properties of the starch fraction

4.1 Functional properties of the SDS and RS

The functional properties of a compound are defined by the way to modify the metabolic patterns, generating a beneficial property. Diverse compounds present in plants show functional properties [2, 49]. In this context, the possible functional properties of SDS and RS have been specially studied in the last years because of their capacity to provide a maintained source of energy avoiding hyperglycemic responses, especially beneficial for diabetic patients. It is important to note that the attenuated glycemic response during starch consumption is dependent on the digestibility behavior that depends on the starch composition and physicochemical properties [50]. The influence on the variability in the glycemic response is considered as an important factor to control the glycemic response in diabetic and obese patients, frequently measured as the concentration of glycated hemoglobin (HbA1c) [51, 52].

Diverse investigations support the evidence of this beneficial effect of the SDS or RS fractions. Hasek et al. [53] studied the effect of the consumption of SDS using obese rats how experimental animal models fed with high fat diet (HFD). A group supplemented with SDS was compared with a group with RDS supplementation. The experimental group fed with SDS reduced the total daily intake of food compared with the RSD group. In addition, when evaluating the expression levels of (mRNA) of hypothalamic orexigenic neuropeptide Y (NPY) and Agouti-related peptide (AgRP), they observed that their expression was significantly reduced in the group fed SDS, as well as an increase in the hormone that produces anorexigenic corticotropin-releasing hormone (CRH). These researchers suggest that SDS can contribute to modulating the frequency of food consumption by activating the gut-brain axis, in addition to generating a reduction in the expression of genes of appetite-stimulating orexigenic neuropeptides and an increase in hypothalamic appetite-suppressing neuropeptide. Therefore, SDS may exert beneficial functional properties.

Breyton et al. [50] compared the effect of the consumption of a diet high or low in SDS in a group of diabetic patients. They observed a reduction in the variability of the glycaemia as well as the lower postprandial area under the curve (AUC) of the glycaemia when the high SDS consumption was considered. These authors consider that the modulation of the starch digestibility may be used as a useful tool for controlling the postprandial glycemic response in diabetic patients. Similar results were reported by Lambert-Porcheron et al. [54], that evaluated the postprandial response and digestibility of a product based on cereals with high or low SDS content in patients with overweight o metabolic risk. They observed a 2 h postprandial glycemic and insulinémica response lower in the group of patients that consumed the product with high SDS compared to the other group.

Considering the effect of RS consumption, diverse studies have reported beneficial effects on human health [11, 12, 13, 26, 50] (Table 2). In this context, the physiological effect of the RS consumption shows a great dependence on the biological origin, the total amount intake and the type of RS consumed [11, 12, 24, 25, 26]. In general, it can be considered that the RS consumption reduces the postprandial glycemic response and improve the glucose metabolism and homeostasis [11, 12, 14, 26] as a consequence of not being digested in the upper human tract [12, 45, 47, 50] and by contributing to a lower but maintained postprandial glucose in the diet [11, 12, 13]. These properties are especially beneficial for type II diabetic patients allowing better control of the glycaemia [11, 12, 13, 26], as well as for healthy individuals [12, 13, 26]. In addition, RS can exert a modulation effect on the satiety by modifying the secretion of adipokines and peptides responsible for this physiological process [12, 13, 26], such as an increase of the release of ghrelin, leptin, adiponectin, glucagon-like peptide 1 (GLP-1), peptide tyrosine (PYY) and gastric inhibitor peptide (GIP). The satiety promotion reduces the total food and calories intake preventing the excess of calories and the accumulation of fatty acids in the adipose tissue [12, 47, 50, 53]. Therefore, RS can be used as a useful tool to prevent and manage obesity [12, 13, 21, 26].

Physiological effect	Mechanism	Beneficial effect
Improve the insulinemic response	The lower digestibility reduces the glucose absorption and glycaemia response	Diabetes; Insulinemic response; Metabolic syndrome
Improve the intestinal epithelial health	Contribute to reverse neoplastic changes on the colon epithelium by the production of organic acids (butyric, propionic and acetic) as a product of RA fermentation.	Colorectal cancer; Ulcerative colitis; Intestine inflammation; Intestinal constipation
Improves the lipid profile	Contribute to reduce the cholesterol and triglyceride blood levels	Cardiovascular disease; Metabolic syndrome; Lipid metabolism
Promote the satiety process	Reduce the total calories intake since RS is not digested in the upper gastrointestinal tract; Promote the secretion of the hormones related with the satiety process	Obesity; Diabetes
Increase the nutrient bioavailability	Improves the intestinal absorption of minerals like intestinal absorption of minerals like iron or calcium	Osteoporosis
Prebiotic effects	Promotes the growth of microbiota bacteria associated with healthy microbiota (Bifidobacteiurm and Lactobacillus)	Colon health; Metabolic syndrome
Dietetic fiber effects	Reduces the atrophy of the colon epithelium, contribute to prevent the intestinal constipation	Improves the intestinal health; Improves the intestinal peristalsis

Table 2.

Physiological effect of the RS consumption.

Other beneficial effect attributed to RS is its capacity to act as a prebiotic compound. Since RS is low or not digested in the upper gastrointestinal tract, it reaches the colon as part of the dietetic fiber [24, 25, 28, 46]. RS is fermented by the colonic microbiota bacteria releasing SCFA, especially butyric acid, an essential compound to maintain the intestinal epithelium permeability and associated with colon cancer prevention. In addition, the SCFA can modulate satiety and lipid metabolism and are also substrates of the intestine gluconeogenesis. This process is associated with a reduction of hepatic gluconeogenesis and therefore a direct impact on the postprandial glycemic response [12, 13, 21, 25, 26, 50].

The prebiotic effect of the RS is associated with the RS fermentation by Bifidobacterias and Lactobacillus species allowing to promote the growth of this beneficial bacteria in terms of total amount and diversity [12, 25, 26]. Dysbiosis, defined as a negative alteration of the microbiota population, is generally associated with a reduction of the microbiota diversity and especially with the alteration of the Bacteroidetes and Firmicutes phyla, characterized in general by the increase of the Firmicutes/Bacteroidetes ratio and the reduction of the Bifidobacterias group. These microbiota alterations are associated with intestinal complications and the increase of the incidence of chronic diseases such as obesity, type 2 diabetes, cardiovascular diseases, and also with cancer [55, 56, 57]. The prebiotic effect of RS promotes the growth of Bifidobacterias and Lactobacillus species, contributing to maintaining a healthy microbiota, a continuous production of SCFA, maintaining the integrity of the intestinal epithelium, and as consequence, reducing the intestinal absorption of bacterial lipopolysaccharide (LPS) and therefore, reducing and preventing the endotoxemia, metabolic stress and chronic systemic inflammation, responsible or contributors of many chronic metabolic diseases [56, 57].

This prebiotic action of RS may exert an effect on glucose metabolism through different mechanisms, such as decreasing the gastric emptying, decreasing the glucose absorption in the intestine, favoring or promoting the production of GLP 1, as well as decreasing the expression in the transcriptional factors that intervene in the oxidation of fatty acids and lipogenesis, generating a decrease in the free fatty acids levels in the blood [56, 57].

4.2 Modulation of the glycaemia homeostasis by SDS and RS

As was exposed before, the nutritional characteristics of starch depend on its structural and physicochemical properties, responsible for the different digestibility, bioavailability, and postprandial glycemic and insulinemic response [4, 14, 15, 19]. Starches with higher SDS and RS fractions show a slower digestibility, progressive assimilation, and therefore a lower glycemic response. Conversely, high RDS contents are characterized by rapid digestion, assimilation and an elevated glycaemic response [19, 44, 50, 53, 54]. Therefore, the starch characterized by high SDS or RS contents can be used to avoid hyperglycemia [19, 26, 44, 45] and get a higher control of the postprandial glycemic response and glucose homeostasis in metabolic syndrome diseases, especially for diabetic patients [13, 54, 56]. The replacement of natural starchy foods by starches with higher SDS and RS content together with the commonly prescribed drug is an adequate strategy to get an integral control of the glycaemia response [4, 13, 15, 19, 26, 44, 47, 50, 54, 56].

Diverse in vivo studies show that RS consumption is associated with benefits in glucose homeostasis [13, 54, 56, 58]. Sun et al. [58] evaluated the consumption effect of RS-II in rats with type 2 diabetes, fed with a diet high in lipids and glucose for 4 weeks. The experimental group showed a reduction trend in glycaemia compared to the diabetic control group (without RS-II). Also, higher glycogen levels were determined in the liver and muscle of the experimental group compared to the diabetic control but similar levels that the non-diabetic group fed without RS-II. Similar results were determined by Zhou et al. [59] when RS from high amylose maize were evaluated during 4 weeks. The experimental group of diabetic rats fed with RS significantly reduced the glucose cholesterol and triglycerides blood levels compared with the control diabetic rats (non-fed with RS) and even HDL levels were determined twice as high in the first group. Zhou et al. [59] and Sun et al. [58] suggest that the biological mechanism responsible for the beneficial RS effects in the glycemic response is mediated by the promotion of the hepatic glycogen and the gluconeogenesis inhibition together with higher efficiency in the glucose intake by the muscular tissue [13, 59]. Gluconeogenesis is the metabolic pathway responsible for the endogenous synthesis of glucose molecules through the use of non-carbohydrates precursor molecules such as pyruvate, alanine, or glycerol. The phosphoenolpyruvate carboxykinase enzyme (PEPCK) converts the oxaloacetate to phosphoenolpyruvate during the gluconeogenesis pathway, whereas during the last step of this pathway the glucose-6-phasphatase (G6Pase) removes the phosphorous group in the 6 positions of the glucose-6-phasphate releasing glucose [13, 60, 61]. Diabetic patients are characterized by continuous activation of the PEPCK and G6Pase enzymes as a response to the low glucose intake by the muscle tissue as a consequence of an inadequate insulinemic response, causing hyperglycemia under fasted state [13, 61, 62]. In this context, diverse in vivo studies have observed a reduced expression of the PEPCK and G6Pase enzymes in diabetic rats treated with RS and therefore, a reduction of the gluconeogenesis activation [58, 59]. The glucose intake by the muscle tissue and the inhibition of gluconeogenesis provokes the activation of the AMP-activated protein kinase (AMPK) restoring the cell energy or ATP. Both mechanisms have been associated with SDS consumption since in vivo studies show the activation of the AMPK with SDS intake [13, 62, 63].

Other authors suggest that the benefits in the glucose homeostasis derived from the RS intake are a consequence of improved lipid homeostasis. The improvement in lipid metabolism is modulated through the promotion of muscular lipid oxidation and cholesterol homeostasis, both related to the improvements in glucose homeostasis. Whereas, other authors suggest that the improvement of the glucose homeostasis is a consequence of the SCFA released, contributing to promote the satiety process and improving the serum lipid profile, both related to an improvement in the prognostic of the insulin resistance [56, 58, 59, 61].

Many researchers suggest that SDS or RS consumption improves the glycaemia in diabetics through the activity reduction of the enzymes of the hepatic gluconeogenesis and the augmentation of the glucose intake by the muscle tissue [58, 59, 61], as well as by the improvement of the lipid homeostasis consequence of the release of SCFA during colonic fermentation of RS [26, 53, 57]. The improvement of glucose homeostasis is an efficient mechanism to reduce the long-term complications consequence of diabetes, mainly related to oxidative stress and cell damage [61, 62, 63]. In this context, the glycemic response in healthy individuals and type 2 diabetic patients is correlated with the type and amount of RS ingested [63, 64]. Other biomarkers related to glucose modulation are the C peptide, leptin, PYY, GLP-1, GIP, and some inflammatory cytokines. The RS consumption is associated with the increase of plasmatic levels of GLP-1, GIP, and PYY, responsible for the insulinemic response, glucose regulation, and satiety process. The released SCFA during RS colonic fermentation could be associated with the increase in the expression of PYY and GLP-1 genes, establishing a relation between RS consumption and intestinal hormones production [63, 64]. Maziarz et al. [65] demonstrated that RS consumption reduces leptin production probably a consequence of augmentation on the fatty acids oxidation since serum circulating levels of leptin are associated with the total body fat mass and negatively correlated with fatty acids oxidation.

5. SDS and RS as potential functional ingredients

As a consequence of the improved awareness of the consumers in the relation of diet and health, the food industry has focused on the production of functional foods based on cereals, legumes, and other products with low glycemic index (GI) [11, 12, 13, 25, 29, 32]. Currently, new sources for RS obtention or production have been investigated as alternatives to the conventional sources (maize, wheat, rice, among others) since RS beneficial effects are dependent on the botanical origin, type of RS, and total intake amount [12, 25, 29, 32]. RS is shown as a great potential functional ingredient because of their great techno-functional properties such as small particle size, color, soft flavor, well properties for the extrusion process, high temperatures of gelatinization, and low water retention capacity, together with their low caloric values (1. 6–2.8 kcal/g) [5, 11, 25]. In addition, may improve the lifespan of dry products and avoid the ice crystals during the ice creams production [5, 25, 29, 46]. These properties allow to incorporate RS as an ingredient in many different food matrixes such as dairy products, bakery products, or pastas [5, 11, 25, 46].

RS can be used also to increase the total fiber content of food products or to reduce the low available CH contents in the production of dietetic food products focused on reducing the bodyweight through a lower caloric content [25, 46]. The incorporation of RS to the food formulation does not change the flavor neither produce significant changes in the texture, whereas may improve the product sensorial properties compared with many available fibers such as brans or gums [11, 25, 46], also, the final product texture can be improved by using RS because of their low water retention capacity [29, 46, 47, 48]. RS has been also used as a cover ingredient during probiotics microencapsulation to be incorporated into dairy products, allowing increasing the viability of the probiotics. Also, RS has been used to encapsulate fish oils to reduce the odor and lipid oxidation [5, 25, 46, 47]. RS can be used in bakery products and breakfast cereals as a functional ingredient and fiber source but attention to the technological properties of the products should be observed to ensure to reach the desirable properties on the product [5, 11, 25, 29, 46]. The addition of RS-III to sourdough breaths may improve the toasted color and the crunch properties of the product [25, 46, 47]. However, the addition of green banana flour (rich in RS-II) to pasta may provoke a weaker mass as a consequence of the gluten dilution effect but less oil is required to fry these products [5, 25, 46]. The addition of RS-III ha can generate in the flour tortillas lower flexibility, rolling capacity, and cohesion. High concentrations of RS-III reduce structural integrity and therefore product quality [5, 25, 29, 32, 46].

On the other hand, the evaluation of the impact and benefits in the consumption of SDS as a functional ingredient for the elaboration of products that improve the postprandial glycemic response has increased in recent years. Rebello et al. [66] evaluated the effect of the consumption of SDS as a functional ingredient in a Snack, with the purpose of improving the postprandial response, the degree of satisfaction, and appetite in people with overweight and obesity. The consumption of the snack with SDS at breakfast improved the postprandial glycemic and insulinemic response by decreasing the concentrations of glucose and serum insulin in the blood per unit of time (minutes), compared to a control product without SDS. In addition, they estimated that the relative glucose responses in the evaluated products were 40% lower compared to the control product. They attribute this effect to the characteristics and type of CH ingested, and to a lower rate of digestion and absorption of the same. These results are consistent with that reported by Péronnet et al. [67], where they evaluated the consumption of a cereal product with different SDS contents (high and low) to evaluate the type of glycemic response in relation to the underlying changes in the kinetics of plasma glucose, on the increase in the rate of production (appearance) and consumption (disappearance) of serum glucose in the blood in healthy young women. They observed that the consumption of the product with a high content of SDS generated a significant reduction in the absorption and consumption kinetics of plasma glucose concentrations, compared to the consumption of the control products. This group considers that the consumption of the product with a high content of SDS generates a slow absorption of glucose, reducing its availability, and promotes a continuous gradual effect, attenuating sudden changes in concentration in the kinetics of plasma glucose, improving its homeostasis.

6. Conclusions

The impact of starch consumption on the human health is dependent on the starch composition and physicochemical properties, highly dependent on the botanical origin of the starch or the processes applied. In this context, the major factor associated with the impact of starch consumption on the human health is the hydrolysis behavior during the gastrointestinal tract, and therefore, with the composition and amount of RDS, SDS, and RS fraction in the starch molecule. Starches with high RDS amounts are characterized by rapid and high glycaemic and insulinemic peaks, being a risk for further diabetes and other chronic diseases. Conversely, SDS and especially RS are associated with low or very low but maintained glycemic and insulinemic responses, and therefore, are associated with benefits for the glucose homeostasis in diabetics but also in healthy people. RS is shown as a promising functional ingredient since this molecule, depending on its morphological structure and physicochemical characteristics, is low or non-digested and shows other potentially beneficial properties. The majority of RS is fermented by the colonic microbiota allowing to growth of the Bifidobacterias and Lactobacillus species, acting as a prebiotic compound. Also, SCFA is released from their colonic fermentation, associated with the increase in the expression of satiety hormones such as GLP-1, GIP, and PYY, contributing to reducing the total calories intake. It has been suggested that RS and SDS consumption is also associated with the glucose homeostasis, contributing to reduce the expression of the gluconeogenic enzymes (PEPCK and G6Pase) and improving the glucose intake by the muscle tissue. In addition, RS and SDS may contribute to lipid homeostasis, increasing HDL release and lipid oxidation. However, more detailed studies are required to clarify the capacity of RS and SDS to modulate glucose and lipid homeostasis. In conclusion, starches with high SDS and especially RS are associated with health benefits such as low insulinemic responses, glucose homeostasis control, prebiotic effects, and satiety, being RS as a promising but low exploited functional ingredient.

Conflict of interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.