a*, pamela c. flores-silvab, edith agama-acevedoa

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eSTARCH DIGESTIBILITY: PAST, PRESENT, AND FUTURE

Luis A. Bello-Pereza*, Pamela C. Flores-Silvab, Edith Agama-Acevedoa, Juscelino Tovar c

a Instituto Politécnico Nacional, CEPROBI, Yautepec, Morelos, México.

bDepartamento de Ingeniería de Procesos e Hidráulica, Universidad Autónoma

Metropolitana-Iztapalapa.

c Department of Food Technology, Engineering and Nutrition, Lund University. Lund,

Sweden

* Corresponding author: Phone: +52 735 3942020, Fax: +52 735 3941896. E-mail:

[email protected]

Abstract

In the last century, starch present in foods was considered to be completely digested.

However, during the eighties, studies on starch digestion started to show that besides

digestible starch, which could be rapidly or slowly hydrolysed, there was a variable fraction

that resisted hydrolysis by digestive enzymes. That fraction was named resistant starch

This article is protected by copyright. All rights reserved.

This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as doi: 10.1002/jsfa.8955

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e(RS) and it encompasses those forms of starch that are not accessible to human digestive

enzymes but can be fermented by the colonic microbiota, producing short chain fatty acids.

RS has been classified into five types, depending on the mechanism governing its resistance

to enzymatic hydrolysis. Early research on RS was focused on the methods to determine its

content in foods and its physiological effects, including fermentability in the large intestine.

Later on, due to the interest of the food industry, methods to increase the RS content of

isolated starches were developed. Nowadays, the influence of RS on the gut microbiota is a

relevant research topic due to its potential health-related benefits. This review summarizes

over 30 years of investigation on starch digestibility, its relationship with human health, the

methods to produce RS and its impact on the microbiome.

Keywords: Digestibility; microbiome; resistant starch; slowly digestible starch; satiety

Starch overview

Starch hydrolysis

Overview

Resistant starch (RS)

Slowly digestible starch (SDS)

Modulating starch hydrolysis


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e Foods (processing and food matrix)

Ingredients (methods to produce RS and SDS)

Structure-digestibility relationship

Health benefits of RS and SDS

Microbiome

Satiety

Conclusions

References

Starch overview

Starch is among the three main polysaccharides present in nature, but in contrast with

cellulose and chitin that are structural molecules, starch is a storage carbohydrate. From a

functional point of view, starch present in cereals (maize, wheat, rice, etc.), legumes (beans,

lentils, chickpea, etc.), tubers and roots (potato, sweet potato, cassava, etc.) and unripe

fruits (plantain, mango, apple, etc.) gives functionality (viscosity, water retention,

mouthfeel, etc) when they are cooked and consumed directly or used to prepare processed

foods as bakery products, tortillas, pasta, etc.1,2 In both forms of consumption, the

nutritional aspect of starch is most important, where the product type (food matrix),

processing (e.g. mixing, cooking type) and other ingredients in the product (lipids,

proteins, polyphenols) have marked influence on starch digestibility and the glycaemic

response.3 Also, starch can be isolated and used as an ingredient in foods, but under this

application type it is mainly used to impart functionality, without paying much attention to

the nutritional aspect. However, in the last decade, there has been interest in the

development of starch ingredients with reduced susceptibility to hydrolysis by digestive


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eenzymes, resulting in slow and limited glucose supply to the circulation. Those foods with

starch of low-digestibility are attractive for people with diabetes and other obesity-related

health problems.

The nutritional value of starch depends on extrinsic aspects, as mentioned above, and

intrinsic features such as granule size, amylose/amylopectin ratio, chain-length distribution

of amylopectin and arrangement of starch components in the granule, which are important

both when foods are ingested as a complex matrix and in the production of starch

ingredients with reduced glycaemic impact.

Starch is a homopolysaccharide of glucose. The polymer consists of two main

components: amylose and amylopectin. Amylose is considered an essentially linear

molecule where the glucose units are linked by α-(1-4) bonds; however, amylose presents

scarce branching points but its functionality corresponds to that of a linear polymer.

Amylose is found in the amorphous lamella of the starch granule. Amylopectin is the

branched component with linear sections where glucose units are linked by α-(1-4) bonds,

and branching points consist of α-(1-6) bonds. Amylopectin is responsible for the

crystalline lamella of the granule, and its branching points are part of the amorphous

lamella. The presence of amorphous and crystalline lamellae in the starch granule confers

this biopolymer a semi-crystalline entity. The semi-crystalline characteristic of starch

granule, i.e. the arrangement of starch components4, is an important determinant of its

digestibility, more than the crystallinity level.5,6. Recently, it was reported that flexible α-

glucans obtained after gelatinization of waxy rice starch are exposed in the periphery of the

granules and are the primary substrate of α-amylase; those flexible α-glucans are rapidly

cleaved in the initial stage of the hydrolysis. However, considering the intrinsic


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eheterogeneity of individual starch granules and the even larger differences observed among

granules of different botanical sources, the mechanisms of the hydrolysis by α-amylase

deserve more detailed investigation, given the important physiological implications of

starch digestion.7

Starches are classified according to the amylose/amylopectin ratio: those starches

with 25-30 % amylose and 70-75 % amylopectin are usually named as “normal” starches;

some starches present high amylopectin levels (98-99 %) and are called “waxy” starches; a

third group includes starches with high amylose contents (50-70 %), e.g. Hylon® maize

starches.

Starch isolated from different botanical sources can present minor constituents, as

proteins, lipids and phosphate groups. Potato starch present phosphate monoesters and

phospholipids that give special functional characteristics to gels made with this starch.

Potato starch gels show high peak viscosity and high transparency attributed to the

phosphate groups present at the branching points of amylopectin. The lipids present in

some starches, such as maize and rice, can form inclusion complexes with amylose and

modify the digestibility of the polysaccharide, since the network produced during gelation

(food matrix) can restrict the accessibility of the polymer to the enzymes responsible for the

hydrolysis process. Also, the interactions between phosphate groups and amylopectin

chains change the starch structure in such a way that it is not efficiently recognized by

amylolytic enzymes, thus becoming a bad substrate.

Starch hydrolysis

Overview


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eThe hydrolysis of starch present in the foods has been a hot topic for more that twenty-five

years (Figure 1). Before, it was accepted that all starch present in foods was hydrolysed,

first by the action of salivary α-amylase and later at small intestinal level by pancreatic α-

amylase, producing, maltose, maltotriose and other branched oligosaccharides called α-

limit dextrins, which are further converted into glucose by the action of the brush border

enzymes maltase-glucoamylase (MGAM) and sucrase-isomaltase (SI).8 Initially, following

an intense period of analytical controversy, a European Concerted Action (EURESTA) was

undertaken5 ,confirming that a significant fraction of starch in foods is not digested and

absorbed in the small intestine, reaching the colon where it is fermented to variable extent

by the microbiome. This fraction was called resistant starch (RS).9 From that moment,

many research groups were interested in the classification of RS types9, methods to

determine RS10-14 and methods to produce resistant starch-rich ingredients15-19 using starch

from different botanical sources and treatments. Starch digestibility is associated with the

proportion of starch that is absorbed as in the small intestine. The kinetic component of

starch digestion is mainly associated with so-called glycaemic index (GI), which has strong

influence on the postprandial metabolism. The GI is used to quantify the postprandial

blood glucose response to starchy foods and it is a tool for their characterization and

classification in terms of the physiological response they elicit.20,21

Resistant starch (RS)

From the publication of a concerted definition of RS as “ the sum of starch and the

products of starch degradation not absorbed in the small intestine of healthy individuals”9

there has been sustained interest on this fraction. Recently, RS was included as part of the

dietary fibre definition and it has been associated with weight management benefits, among


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eother potential effects. Diverse reviews on RS have been published over the years. Most

recent publications classify RS in five different categories:22-25

RS1: physically inaccessible starch, i.e. entrapped in a mechanically resistant cellular

matrix.

RS2: native starch granules (raw) with particularly organized structure.

RS3: retrograded starch, produced after cooking and cooling of starchy foods

RS4: chemically modified starch, with the formation of “new” chemical bonds.

RS5: amylose-lipid complexes and resistant maltodextrins.

Englyst et al.11 classified starch digestion according to the rate and extent of its hydrolysis

after ingestion. Following their in vitro methodology for the evaluation of starch

digestibility, the fraction that resists a 120-min hydrolysis treatment was classified as RS.

Such a cut-off was introduced by comparison with in vivo digestibility estimations in

ileostomy patients. Controversies emerged when RS was included in the dietary fibre

concept since it is suggested that the food should be analyzed “as eaten” i.e. without

additional heating that disorganizes the starch structure (gelatinization), as indicated in the

official method. The basis for this proposed modification is that upon heating granular RS

fractions become available starch and is therefore not determined as part of dietary fibre.

Also, 4 h instead of 16 h of hydrolysis by the enzyme cocktail was proposed to better

mimic physiological conditions during digestion26 but, evidently, further studies of these

aspects are necessary.

In our opinion current trends in RS investigation include the use of alternative starch

sources (e.g. banana) and methods to produce RS-rich powders that can be used as

ingredient in foods with high indigestible carbohydrates content; the effect of the food

matrix and starch interactions with diverse macromolecules and polyphenols that restrict or


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einhibit starch digestion and absorption of the released glucose; the relationship between RS

structure and digestibility with application in the development of tailor-made starches; the

relationship between the intake of RS and gut microbiota composition and metabolism and

its connection with the host health. These topics will be addressed in the following lines.

Slowly digestible starch (SDS)

The Englyst’s classification of starch fractions based on the hydrolysis rate and extent also

considered a fraction that is slowly digested thus resulting in sustained glucose release in

the small intestine. The importance of this fraction, named SDS (slowly digestible starch),

resides in that its ingestion results in no sharp postprandial blood glucose peak with a

concomitant low insulinaemic response; the control of glycaemic and insulinaemic

postprandial responses is an issue of relevance for both diabetics and healthy people. The

slow digestion feature of this starch fraction of foods is related to many factors, such as

structural changes produced during processing, cooking and storage. Zhang and Hamaker27

proposed two fundamental mechanisms involved in the slow digestion of starch: a)

modification of starch structure that decreases enzyme susceptibility; b) change in the

starch structure that limits the rate of enzyme hydrolysis. In addition, certain structural

characteristics of the food matrix are also relevant, as those represented by a limited

physical accessibility of starch due to its entrapment within rigid cell walls in legumes,28 a

phenomenon that has significant analytical and physiological consequences.29-31 Zhang and

Hamaker27 have stated that there is no in vivo method capable of evidencing the real SDS

content of foods. By definition, SDS is slowly digested resulting in sustained glucose

liberation throughout the whole length of the small intestine. SDS is thus considered a

nutritional concept that is quantified as a physiological response. These characteristics


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ehamper a relevant in vitro quantification of SDS, keeping in mind the complexity of the

human body response to dietary carbohydrates. As a matter of fact, the current in vitro

quantification of the various fractions comprising the digestible starch content of foods has

been questioned recently,31 proposing that the nutritional classification of starches should

be modified with attention to parameters derived from advanced kinetic analyses of starch

digestion, instead of relaying on in vitro RDS, SDS and RS measurements only. As

consumption of low glycemic index foods, i.e. those rich in SDS, begun to be increasingly

associated with improved intestinal and systemic health, more investigation was necessary

to improve the quantification of this fraction. In this sense, Zhang and Hamaker27 proposed

the extended glycaemic index (EGI) concept to determine in vivo the extent of glucose

release over a prolonged period of time in different foods and SDS-rich ingredients. Also,

the authors proposed the EGI to evaluate the nutritional characteristics of foods on the basis

of their glycaemic carbohydrate content.

Modulating starch hydrolysis

Foods (processing and food matrix)

The unit operation for food processing (traditional and novel) can be manipulated to control

the starch digestion present in different foods, such as bakery products, pasta, snacks,

parboiled rice, potato, breakfast cereals, cooked beans, etc. Also, storage conditions can

modify starch digestibility. Food processing involves gelatinization of the starch present

which later undergoes a re-ordering of its polysaccharide components, a process that starts

immediately upon cooling. During this re-ordering, generally named “retrogradation”,

amylose chains lixiviated from the starch granule in the gelatinization process, are

organized in a parallel or elongated arrangement, a phenomenon that is potentiated by


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estorage. This arrangement produces a structure that is refractory to the action of digestive

enzymes and thus contributes to the RS fraction. Also, native (ungelatinized) starch

granules can contribute to the overall RS fraction present in a food. The thermal processing

of starchy foods in the presence of lipids can produce amylose-lipid complexes that also

form part of the RS fraction. The presence of diverse components in the food matrix, such

as proteins and lipids that can interact with starch, modify the digestibility of the

polysaccharide and the sensory characteristics of the products. For example, bread baked

from just wheat flour, salt, water and yeast, becomes retrograded upon storage, a process

that is easily noticed by the increased hard texture of the bread; however, on the other hand,

bread baked using lipid ingredients undergoes slow retrogradation, as consequence of the

more limited interactions occurring between gelatinized starch chains. Nonetheless, the use

of lipids leads to the formation of amylose-lipids complexes, with reduced starch

digestibility. Partially gelatinized starch is frequently present in foods. It retains the

crystalline structure (mainly cereal starches with A-type) and contributes to SDS fraction.5

The presence of non-starch polysaccharides (e.g. cellulose, hemicellulose, gums), proteins

and lipids in the food matrix can decrease the access of the digestive enzymes to gelatinized

starch and results in slow digestion. Cooked legumes, such as common beans, contain

partially gelatinized starch granules entrapped by mechanically resistant cell walls which,

as mentioned earlier, restrict amylolysis with concomitant slow digestion. The border

between RS and SDS fractions is not completely defined and depends on diverse extrinsic

factors as chewing time, foods included in the meal, characteristics of the digestive system

(diseases, drug treatments), etc. The physical structure of the food matrix is another

characteristic that may contribute to a slow digestion of starch and may be controlled


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ethrough the cooking degree. Pasta, for instance, exhibits a dense and compact structure that

results in a remarkable slow starch digestion rate and glycaemic response.32,33

Ingredients (methods to produce RS and SDS)

The first strategy to produce a RS-rich powdered ingredient included the use of high-

amylose maize starch and repeated heating-cooling cycles; this process involves structural

disaggregation of linear chains that are reorganized in a new structure that is resistant to

hydrolysis by digestive enzymes. In the same sense, RS production has been achieved

through the generation of α-glucan linear chains by means of debranching enzymes, as

isoamylase and pullulanase that hydrolyze α-1-6 bonds in amylopectin, and can be later re-

arranged in a retrograded structure. The introduction of chemical groups in the starch

structure also increases the RS fraction. Chemical modification of starch as crosslinking,

acetylation, oxidation, hydroxypropylation, esterification and combinations of them

produce RS;34-37 however, the level of reagents used in these modification processes is

regulated and therefore the chemical approach is not easy to implement. Physical

modification of starch, as for instance by hydrothermal treatments where annealing is

included, has been used to produce RS. Annealing implies an excess of water (> 65% w/w)

and temperatures below the gelatinization point but above the glass transition

temperature38, conditions used to destroy the granular structure resulting in rearrangement

of the starch structure that is responsible for enhanced resistance to enzymatic hydrolysis.

Heating-cooling cycles are used to increase the RS content in high-amylose starch.16,39 The

repeated heating of a starch dispersion produced disaggregation and breaking of both starch

components (amylose and amylopectin) in shorter chains. After, the cooling down of the


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eshorter starch chains leads to the formation of double helices aggregates, favoring the

formation of denser but smaller crystals, increasing in this way the RS content.40 The

retrogradation (reorganization) of starch chains leads to the formation of RS fractions. The

process involves three steps, namely, nucleation by intra-molecular initiation of ordered

chain helical segments, propagation by the growth of crystals from the nuclei by the

association of chain segments, and maturation by crystal perfection.41

RS-rich powders can also be produced by inducing the formation of amylose-lipid

complexes. High-amylose starch was heated, cooled and incubated with isoamylase to

produce linear chains and complexed with a fatty acid (palmitic acid). The RS content in

the powder, assessed as dietary fibre, was 53% and was attributed to the presence of both

retrograded starch and amylose-lipid complexes; the RS-rich powder was included in a

bread that induced lower postprandial plasma-glucose and insulin responses compared with

a control bread.18 The use of conventional starches to produce RS-rich powders involves a

combination of methods. Chemical (acid treatment), cooking, extrusion and hydrothermal

treatment were required to produce a RS-rich powder from “normal” maize starch, as its

structural features (mainly amylose/amylopectin ratio) do not allow for producing

enzymatic hydrolysis-resistant entities in a single step.17 A recently review discusses RS

preparation using different methods and factors that influence RS formation.24 These

methods have been applied to starch isolated from diverse botanical sources35,42,43; the

application of any method, or combinations of them, aiming to increase the RS content

depends mainly on the specific use planned for the starch powder (e.g. cooking ingredient

or ready-to-eat product).

There is interest to modify the starch structure present in starchy flours, avoiding the

isolation step for the production of a low-cost ingredient. Unripe plantain flours were


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eproduced after cooking of the fruit for 5, 15 and 25 minutes in boiling water; the flours

showed a decrease in RS content (around 25%). For this reason, two treatments of the

flours were tested to increase the RS content. Plantain flours were modified with thermal

treatments using 30% moisture content at 120 °C for 24 h; the effect of cold storage (– 20

°C, 7 days) was also investigated. The raw flour analyzed according to Englyst et al.11

protocol exhibited a high RS content (65.6%), which did not change with the thermal

treatment (63.6%) and the additional storage (65.1%). The second treatment (annealing) of

the flours showed similar RS content, suggesting that the remaining starch structure was

similar after both thermal treatments. Although a decrease in RS content was observed,

these unripe plantain flours may be used directly in food applications that do not require

additional cooking, e.g. smoothies, salad dressings, breakfast cereals, etc, to increase the

indigestible carbohydrate content.44,45 Thermal treatments (annealing and high-moisture

treatment) were applied to brown rice flour and no significant change in the molecular

structure was found. This pattern can be related to the matrix in the rice flour (proteins and

non-starch polysaccharides) that protect the starch granules during thermal treatment. After

the treatments, starch was isolated and analyzed to evaluate the changes in its structure. The

molecular weight of the polysaccharide in the treated samples showed a slight decrease

without change in the average chain length; a slight disorganization in the double helices of

amylopectin chains was evidenced by a decrease in the relative crystallinity and enthalpy

value, assessed by differential scanning calorimetry. The granular -uncooked- starch before

the Englyst’s test showed RS content between 11 and 16%, which can be considered low;

however, this RS level was retained after gelatinization of the preparation, suggesting that

the flours can be used in the formulation of foods that require cooking.46


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eMultiple research groups around the world have been working on physical and enzymatic

treatments to increase the SDS fraction. Starch structure modification with amylosucrase

enzyme involves elongation of the non-reducing ends of (1—4)-α-glucans with sucrose as

substrate; the change in the starch structure causes amylolytic enzymes to hydrolyze the

starch substrate slowly -or not at all- since both SDS and RS fractions are produced.47-50

Hydrothermal treatments, specifically heat-moisture treatment, are used to modify the

starch structure and produce SDS. Native potato starch was adjusted to different water

contents (20, 50 or 90%) and oven-heated at 40, 55 or 100 °C for 12 h. It was found that the

hydrothermally treated samples showed crystalline arrangement, which changes from Cb-

type to A-type and a short-range order was observed by differential scanning calorimetry

(DSC) due to the phase transition in excess water. Two basic crystalline arrangement types

are found in natural starches: A-type is due to arrangement of short chains and B-type to

long chains; the C-type is a mixture of A- and B-types and it is subdivided in Ca-type or

Cb-type, depending on the predominant crystallinity feature (A- or B-type, repectively).

The highest SDS yield was recorded after treatment with ≥ 50% moisture content at 55 °C.

However, more investigation will be needed in order to produce a more heat-stable SDS

ingredient that can be used in formulations requiring additional processing.51 Optimal

conditions of heat-moisture treatment to produce SDS were evaluated in waxy potato

starch, reporting 41.6% SDS content following a treatment at 25.7% moisture content at

120 °C for 5.3 h.52 The study showed structural changes in the crystalline arrangement from

B-type to a combination of B- and A-types, as well as the presence of more imperfect or

heterogeneous crystallites which may be due to the broadened phase transition observed by

DSC after treatments in conditions of excess of water. These alterations have been related


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eto the change in starch digestion rate. More recently, there has been efforts to produce SDS

ingredients that can be released and hydrolysed distally, i.e. in the ileum section, in order to

activate the ileal brake involved in the regulation of the gastric emptying rate; when the

gastric emptying rate is low (associated with the consumption of SDS) the glycaemic

response is moderate and may beneficially impact satiety.53,54


It is well-known that the above-mentioned treatments modify the original structure and the

arrangement of starch components in both amorphous and crystalline lamella. Structural

changes modify the starch digestion but also alters its functionality (e.g. low retrogradation,

low syneresis, high water retention, etc). When applied individually or in combinations for

the production of a food ingredient, these treatments generate changes in starch structure

that impact its digestibility to a variable extent. For example, the slow digestion features of

starch have been related to the granular X-ray diffraction pattern, chain-length distribution

of amylopectin chains (short/long chains ratio), granule shape and size.55 Similarly, the

information of the slow digestion (SDS) characteristic of raw cereal starches

(ungelatinized) and the resistance to hydrolysis (RS) of raw tuber starches are related to the

chain-length distribution.6 Amylopectin in raw cereal starches is generally characterized by

its high content of short chains with high level of branching points, whilst tuber starches

show more abundant long chains; however, a parabolic relationship between short/long

chains ratio and SDS content was found,56 meaning that if a particular starch shows a high-

level of short chains it will show high SDS content, but if long chains are present in a high

proportion a high SDS content will be observed also. This issue deserves more

investigation to elucidate this structure-digestibility relationship.


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eStructural changes produced by chemical reagents, where different functional groups are

introduced, lead to reduced digestibility as digestive enzymes have lower affinity for the

the modified starch substrate. The impact of the chemically modified starches on the starch

nutritional features in the overall diet is low due to the low concentration of modified

starches used in food applications. Pyrodextrinization reactions are used to modify starch

structure by introducing new glycosidic bonds (β-1-3 and β-1-6); this reaction involves

incubation of dry starch with mineral acids at high temperature, yielding a soluble starch

viscous solution57 Pyrodextrinization can be achieved during baking of starchy foods with

low moisture content, producing an increase in the RS content, an issue that should be

investigated taking also into consideration the influence of the food matrix. Debranching of

starch with enzymes (e.g. pullulanase) produce linear chains (amorphous areas) and

residual crystalline sections rich in alpha-glucan double helices, which are organized in

layered structure; this de novo arrangement of starch structure has been associated with

slow digestion properties; intrinsic characteristics of starch (amylose/amylopectin ratio and

chain-length distribution) play an important role in the re-arrangement of starch

components after debranching.21,58-60 We emphasize that depending on structural

characteristics of a particular native starch (e.g. X-ray diffraction pattern), debranching and

subsequent aggregation and arrangement of linear chains in double helices produce

crystalline structures that differ from those originally found in the native starch; this new

entities cannot be hydrolysed by digestive enzymes, which results in increased RS

fractions. In this sense, studies on the structure of native waxy rice starches and its

relationship with digestibility showed that intrinsic characteristics, such as granule size,

the presence of pores in the granule surface, crystallinity degree and chain-length


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edistribution of amylopectin, are important determinants of the resistance to enzymatic

hydrolysis.61 Changes in the crystalline structure due to acid hydrolysis and subsequent

esterification to produce cross-linking between short amylopectin chains originate changes

in starch structure that also result in increased RS contents.62 Cooked rice is a common food

matrix where protein and starch are the main components. In the cooking process of rice,

starch suffers changes in structure that modify its digestibility; it was reported that

amylopectin present in rice starch with long and intermediate chains favour a structure that

resists enzymatic hydrolysis compared with rice starch with higher level of short chains.63

The information generated by studies on structure-digestibility relationship can be used to

propose processes to elaborate starchy foods (food matrix) with specific structure and

digestibility; also, the development of starch powders with RS and SDS using different

methods (single and combined) can be proposed to obtain new ingredients for foods. This

issue is important due to the growing interest to produce foods with reduced and slow

starch digestion features that are associated with potential use in the prevention of diverse

diseases as colon cancer, type 2 diabetes, and cardiovascular problems.

Nutraceutical effects of SDS and RS

So far, our revision has led us to the conclusion that starch nutritional quality strongly

depends on starch structural features and on their changes with processing. Now, we will

discuss the potential nutraceutical effects of SDS and RS consumption, a research area of

intense current interest. It is known that SDS benefits are associated with a low glycaemic

index (GI), which is related to the reduction of the risk of diverse chronic degenerative

diseases such as type 2 diabetes, overweight and other obesity-related disorders.64 Ongoing

investigations evaluate the potential anti-inflammatory and oxidative stress-modulating


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eeffects of SDS-rich regimens.65 However, recent reports have highlighted the importance of

the particular small intestinal location where SDS is digested and its glucose is liberated

and absorbed. Apparently, distal digestion can trigger an ileal brake mechanism that slows

the stomach emptying rate. SDS intake has the potential to stimulate incretin hormone

secretion, which is related to decreased gastric emptying, reduced food intake and increased

satiety.66 Such effects extend nutrient delivery to the body and may decrease appetite and

promote weight management; however, efforts should be focused on developing well-

designed clinical studies to corroborate these results and the minimal dosages required to

achieve them. Considering the complexity of the study needed, and the multiple

mechanisms to contemplate, we anticipate that the first step to accomplish this would be to

develop “in vitro” and “in vivo” consensual methods for SDS quantification. An in vivo

method could be used for a better understanding of the SDS concept and its physiological

effects, and as a tool to study food quality; however, additional questions brought forth by

the EGI concept as length of measurement time, relationship between EGI and GI, and the

response of the regulatory hormones during the extended period, should be primarily

addressed.

The other fraction with health benefits (RS) has the ability to modulate postprandial

glucose rise67-71 and insulin sensitivity,68,70,72,73 indicating that RS could be useful for

managing diabetes. However, the role of RS in metabolic responses is still an issue under

study since there is not sufficient evidence suggesting effects on other metabolic markers

such as blood pressure and plasma lipids.70,74,75 Even though, the evidence from animal

models indicating that RS improves a variety of metabolic features76-78 suggests that,

although these benefits likely arise from a multitude of mechanisms, the gut microbiota is

one of the underlying key factors.79-82 Studies in rats showed that RS may modulate the


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eratio between the two major phyla present in the colonic ecosystem, Bacteroidetes and

Firmicutes, by supporting the growth of beneficial bacteria77 that initiate the degradation of

complex substrates, such as resistant starch particles, yielding beneficial compounds, e.g.

short chain fatty acids (SCFA) (Figure 2). The effect of RS type (RS2 and RS4) on gut

microbiota was evaluated in a double-blind crossover intervention in healthy young adults

showing that both RS types increased Actinobacteria and Bacteroidetes phyla and

decreased Firmicutes; however, RS2 increased the abundance of Ruminococcus bromii and

E. rectale, and RS4 consumption was associated with increased Bifidobacterium

adolescentis and Parabacteroides distasonis.83 This ability of RS to modify colonic

microbiota and SCFA production is also of interest due to the physiological and metabolic

impacts of these metabolites with implications on human health.84 Several in vitro (cell

lines) and in vivo (rat model) studies have related SCFA to systemic effects, not only on

glucose and lipid metabolism but also as key in the prevention and treatment of the

metabolic syndrome, bowel disorders, and colon cancer.85-87 It was found that dietary fibre

protected against colorectal cancer in a microbiota and butyrate-dependent manner.88 Also,

it has been demonstrated that RS feeding produced protection against colitis-associated

colorectal cancer, an action that that was related to significant changes in the gut

microbiota, leading to increased short-chain fatty acids production, mainly butyrate.77

However, it is perhaps unsurprising that effects of RS on SCFA production reported in vitro

and in animal models are not replicated easily in human studies. Such discrepancies are

attributed to the type and dose of RS, the food matrix in which RS is incorporated, the

variability of responses among individuals, and the differences in microbiota composition,

aspects that should be considered for future design of studies. However, it seems clear that

a RS-rich diet can lead to the establishment of a healthy gut microbiota and the


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eunderstanding of how RS interacts with gut bacteria is rapidly advancing; in this sense,

further investigation may lead to classification of RS as a prebiotic.25 Future studies

investigating the influence of RS on human health, should also consider the period of

dietary changes and the fact that biological information is bidirectional, implying therefore

the need of omic sciences and technologies to fully understand postprandial and longer

term effects of RS consumption.

Conclusions

Initial reports indicated that starch present in foods was completely digested and absorbed,

a concept that led to starchy foods restriction for people with diabetes and obesity.

However, it was later discovered that different starches may be digested at different rates or

not digested at all in the human small intestine. Rapidly digestible starch produces a rapid

and sharp postprandial increase of glucose in the blood and it is therefore not recommended

for people with the above-mentioned health problems. Slowly digestible starch (SDS) and

resistant starch (RS), on the other hand, have been associated with some health benefits,

such as low glycaemic and insulinaemic response, satiety and, for RS in particular, the

potential prebiotic effect due to its fermentability by the colonic microbiota, leading to the

production of short-chain fatty acids. Chemical, physical and enzymatic methods for

producing SDS and RS with specific structure give the possibility to taylor-made both

fractions with health benefits. Current investigations are directed to finely determine the

location of glucose release after hydrolysis of SDS in the small intestinal lumen, and the

effect of RS fermentation on differential growth of particular bacteria group in the human

colon.


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e

Acknowledgements

The authors thank the CONACYT-Mexico, SIP-IPN, COFAA-IPN and EDI-IPN for

support.

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eFigure legends

Figure 1. Starch digestibility knowledge trough time. Slowly digestible starch, SDS;

resistant starch, RS.

Figure 2. Resistant starch effects on gut health.

Starch is completely digested;

however at different rates

A starch fraction resists hydrolysis by

digestive enzymes Methods to

analyze and increase SDS, RS fractions

PAST PRESENT FUTURE

Physiological effects,

connection to gut health and

microbiota


Figure 1. Starch digestibility knowledge trough time. Slowly digestible starch, SDS; resistant starch, RS.


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BacteroidetesFirmicutes

Butyric acid

Colon cancer risk

Bacteroidetes

Firmicutes

Resistant starch

Figure 2. Resistant starch effects on gut health


a*, pamela c. flores-silvab, edith agama-acevedoa

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