Designing food structure to slow down digestion in starch-rich products

Designing

food

structure

to

slow

down

digestion

in

starch-rich

products

Nicoletta

Pellegrini

,

Elena

Vittadini

and

Vincenzo

Fogliano

Thecategoryofstarch-richfoodsisonthespotforitsroleinthe

developmentofobesityandrelateddiseases.Therefore,the

productionoffoodhavingalowglycemicindexshouldbea

priorityofmodernfoodindustry.Inthispaperthreedifferent

fooddesignstrategiesthatcanbeusedtomodulatetherelease

ofglucoseduringthegastrointestinalprocessofstarch-rich

foods,areillustrated.Thestructureofthestarchgranulescan

bemodifiedbycontrollingprocessingparameters(i.e.

moisture,temperatureandshear)thusinfluencingthe

gelatinizationandretrogradationbehavior.Theintactnessof

plantcellwallshinderingtheaccessofamylasestothestarch

granulesandtheformationofastiffedfoodmatrixusingthe

crosslinkingbetweenproteinsandthemelanoidinsgenerated

byMaillardreactionarealsoveryeffectiveapproaches.

Followingthesefooddesignstrategiesseveralpractical

approachescanbepursuedbyfooddesignerstofindreliable

solutionscombiningtheconsumersrequestofpalatableand

rewardingfoodswiththepublichealthdemandofhavingfood

productswithbetternutritionalprofile.

Addresses

1_{FoodQualityandDesigngroup,WageningenUniversity,The} Netherlands

2_{SchoolofBiosciencesandVeterinaryMedicine,Universityof} Camerino,CamerinoMC,Italy

Correspondingauthor:Fogliano,Vincenzo(vincenzo.fogliano@wur.nl)

CurrentOpinioninFoodScience2020,32:50–57

ThisreviewcomesfromathemedissueonFunctionalfoodsand nutrition

EditedbyAndreasSchieber

https://doi.org/10.1016/j.cofs.2020.01.010

2214-7993/_ã2020TheAuthors.PublishedbyElsevierLtd.Thisisan openaccessarticleundertheCCBYlicense(http://creativecommons. org/licenses/by/4.0/).

Introduction

Thebadnutritionalqualityofindustryproductsisatthe very center of the societal debate, and the correlation

between their excessive consumption and the obesity

pandemic has been put forward by several authors [1]. One of themain concernsisabout industrialfoods for-mulations:inmanycases,pillarfoodslackofsomespecific nutrients whileothers are too abundant. To tackle this point,reformulationstrategieshavebeenimplementedin

thelast10yearstoreducethepresenceoffreesugars,fats,

salt and to increase the amount of proteins, vitamins,

dietary fiber, and phytochemicals. A second, subtler,

concernisrelatedto thedegreeof processing:the nota-tionof ‘ultraprocessed’foodswasintroducedtoindicate theexcessiveuseofrefinedingredientsandtheextensive thermaltreatmentscausingmicronutrientslossand favor-ingfastnutrientsuptake[1].Althoughabetter

digestibil-ity was considered a plus of the food processing until

some years ago, in the present obesogeniccontext, the

fast calorie uptake, especially from starch-rich foods, turnedtobeoneofthemaindisadvantagesofthe West-erndiets[2].

Despite the fact that human metabolism is based on

glucose hydrolysis, the wide availability of starch-rich foodcamerelativelylateinhumanevolution:the discov-ery of agriculture and the cultivationof cereals can be

datedonly 10–20 thousandyears ago. Before thattime,

thehunter gathered-man collectedsome starchytubers

andcookedthemonfire[3].Insomecases,thesetubers provided a significant contribution to the total caloric intake,howeverthedegreeofprocessingwasalwaysvery limited. After grain domestication (wheat, corn, rice or milletinthedifferentpartoftheworld),grainrefininghas

been always very limited and the adoption of ‘white

bread’ was traditionally limited to a restricted number ofwealthypeople[4].After theSecond WorldWar,the

abrupt switchtowarda modernfood productionsystem

brought a wide availability of industrial foods rich in refinedfloursand fully gelatinizedstarch. White bread, tortillas,maizeporridgeandothercereal-basedproducts

became the major contributors to the calorie intake of

whatwecall‘Western diet’,whichis considereda hall-markforanunhealthydiet.Inmostofthesefoods,starch hydrolysisduringthegastro-intestinaldigestionis

partic-ularly fast and in some products the starch becomes

metabolically similar to free sugar with well-known

negativeconsequencesonconsumer health.

Thefaststarchdigestioninthesmallintestine,its

imme-diateabsorptionand theconsequent peakof blood

glu-cose, and in turn the fast release of insulin, together

constitute one of the main causes of weight gain and

type2diabetesinsurgence.Moreover,inindustrialfoods design,starchisoftenusedas matrixtoincorporatefats andfreesugarsresultinginhigh-caloriedensefoods[5]. Unfortunately,formostpeopleitisextremelydifficultto resistthetemptationofeatingtoomuchofthesestarch-rich

foodsalwaysavailableataveryaffordableprice.Allthese

factors together contribute to establish the so called

‘obesogenicenvironment’ofthemodernsocieties,which

clearly explains the overwhelming spread of obesity

pandemic.

Different strategies are currently pursued to face the

issue: consumer education, enforcement of restrictive

policies and food reformulations are the most obvious

[6].Unfortunately, alltogethertheyproducedonly lim-itedresults thusfar.

This review will deal with afood technologyapproach

aiming at designing starch-rich foods having reduced/

delayedstarchdigestibility.Thegoalistoobtainproducts thataresimilartotheconventionaloneswithout

substan-tially changing consumers’ sensory experience. This

allows to target those consumers who are not sensitive

to education campaignsand not willingto change their

foodchoicesordietaryhabits.Thistypeofconsumersis veryattractedbythesensorycuesofenergy-dense

starch-rich foods such as the cooked flavors and appealing

textures. They strongly prefer foods that are soft and

palatable, or crunchy and airy, having the common

denominator to be easily masticated and rapidly

swal-lowed.Mostofthestarch-richfoodshavingthesefeatures haveahighspeedofcaloriesingestionpreventingsatiety stimuliandinevitablyleadingtotheintakeofan exces-siveamount offood[7].

In this framework, food designers’ goal should be to

developstructuresthatcandelaystarchdigestionwithout compromisingthedesiredsensorycharacteristicsandthe

characteristic features of the food expected by the

consumers.

In this paper, three strategies to achieve this goal are discussedillustratingtheexistingfindingsandsuggesting

possible futuredevelopments.

Modulate

starch

structure

in

starch-rich

food

It is well known that native starch is assembled into

relatively ordered granular structures. Upon heating in the presence of water, starch granules undergo an

irre-versible structural change, named gelatinization, that

resultsinanamorphousmacromolecularassembly.Starch

gelatinization has very important implications on food

textureasitisassociatedtotheformationofaviscousgel

wherestarchmoleculeshaveadis-orderedconformation

and arelatively high molecular mobility [8]. The open andflexiblemolecularconformationofgelatinizedstarch

makes it accessible to amylases with the consequent

glucose release.

From a nutritional perspective, the ability to control

starch digestion is extremely important to design food

with desired characteristics: the key to control such

process is to modulate the accessibility of enzyme to

itssubstrate.

Foodformulation,processingandstoragevariablesmust allbeconsideredintheirrelevancetofavor/hinderstarch hydrolysis. To slowdown starch digestion all strategies thatlimitattainmentofaflexible,continuous,andmobile

gel and favor the formation of rigid, aggregated, low

mobility, and not accessible structures should be

considered.

Ingredients selection should move toward vegetables

having starch with large, non-porous granules. A high

amylosecontent(smallersurfaceareapermoleculethan amylopectinlimitsamylolyticattack),longbranches,and typeBcrystallineconformationsareotherfeatures delay-ingamylasesaction[9–12,13,14,15].

Alsotheconcentrationofwaterpresentinthefoodbefore

thermal treatment should be carefully considered, as

watercontentisacriticalfactordeterminingthedegree of starch granule swelling, gel formationand structural/ molecularmobility[10].Morecomplexfoodformulations maybepreferredasproteinandlipidsmayinteractwith

starch by means of weak and steric interactions (e.g.

glutennetworkformationandamylose–lipidcomplexes)

forming complexes that diminish starch digestibility

[9,10,13,16,17].The presence of hydrocolloids, dietary fiber,andthickeningagentshasalsoanimportantrolein limitingstarchhydrolysisbyadualmechanism:limiting gelatinizationbysubtractingavailablewaterand increas-inggelviscosity[18–22].However,notalltypesof fiber havethesameefficacyinreducingthestarchdigestibility [18,20].

Food processingvariableshavingaparamounteffecton

starchstructurearetemperatureandshearingconditions,

as schematically summarized in Figure 1. Temperature

increase is necessary to induce starch gelatinization, a processthatbeginswithswellingofstarchgranulesand, eventually,endswiththeirdestructionandtheformation ofacontinuousandflexiblegel.Inthepresenceoffully gelatinizedstarch,molecularandstructuralmobility,free volume,andflexibilityofthegeldeterminetheeasiness

of theenzymetoreach itssubstrate.Homogeneousand

continuous gels guarantee a high accessibility, while

limiting heat transfer andreducing availability of water can restrict starch gelatinization and preserve partial structuralintegritywhileprovidingdesiredtextural mod-ifications [9,10]. A gel containing starch only partially

gelatinized (e.g. containing native and swollen starch

granules in a gelatinized matrix) is less digestible than a fully gelatinizedstarch without necessarily impact on thesensorycharacteristics.

Coolingandstoragetemperaturehavealsoanimportant

retrogradesre-associatingin ordered/crystallineforms.It iswelldocumentedthatamyloseretrogradesmoreeasily andfaster(minutes)thanamylopectin(hours,days)[17]. Moreover,amylosetendstoretrogradeasresistantstarch whileamylopectinas slowlydigestible starch.To maxi-mizestarch retrogradation,starch shouldbeheated and

hold at temperatures between the glass transition and

gelatinizationonsettemperatures(annealing)orbestored atrefrigerated temperatures[13,16,23,24].

Processing techniques operating at low temperatures

(below gelatinization temperature) can be very useful

inproducingfoodswithnon-gelatinizedstarch. Techni-quessuchassprouting,germination,malting,andsoaking

cause a de-structuring of natural assemblies, but the

increase of starch digestibility is lower than the one

obtainedwithgelatinization[9,25].Moreover,ifcoupled

with an acidifying technological step (i.e. sourdough

fermentation),thesetechniquesmaypromoteinteraction

betweenstarch and proteins (gluten)and reduce starch

bioavailability[25,26].Highhydrostaticpressure proces-singisaverypromisingtechniqueforthedesigning low digestible starch products.: it operates at relatively low temperaturesandcausespartial gelatinizationand pres-ervation of starch granule integrity, favors spontaneous retrogradation(resistantstarchformation),andamylose– lipidscomplexation [16,27,28].Finally, evenwhen

pro-cessing techniques operating at high temperatures are

used(i.e.boiling,pressurecooking,frying,puffing, flak-ing,popping),theformation oflessdigestiblestructures maybefavoredbylimitingwateravailability(i.e.baking

of cookies), promotingamylose–lipid complexes

forma-tion (i.e. frying), or enabling fast heating and cooling cycles(i.e.microwaveheating) [9,25].

Shear hasalso a detrimental effect on starch structural

elements and can be modulated to influence them at

differentlevels.Lowshare(i.e.gentlemixing)maycause structuralmodificationsofproteins–lipidspresentinthe grainsbuthaslittleeffectonintactstarchgranuleswhich

Figure1

Current Opinion in Food Science

Schematicrepresentationoftheeffectofprocessingonnativestarchstructures(nottoscale).Thefigurehighlightstheeffectoftemperatureand shearonmajorstructuralcomponentsofnativestarchandthemultiplestarchstructuresthatmaybefoundinthefinalproduct.

Coatedstarchiscoveredbyalipidoraproteinlayer.Entrappedstarchreferstothegranulessurroundedbycellwallorbyanartificialprotein networkcreatedduringprocessing,asithappensindrypasta.

preservetheirstructure.Ononehand,theformationofa

coherent andcontinuous amorphousmatrix(e.g. gluten

network) around starch granules may act as barrier to

enzymaticattach(e.g.pasta)[29].Ontheotherhand,the removal of proteins/lipids onthe starch granule surface

mayhaveaneffectinexposingstarchporesandmaking

them accessible to amylases. High shear (i.e. milling,

extrusion) may have very different effects on starch

properties depending on processing variables such as

water content,energy, temperature and duration.In an

effort to minimize starch digestion, milling should be

modulatedtominimizestarchgranulesbreakage, separa-tion of proteins and lipids from granule surface,and to controlthedegreeofde-branchingofstarchmoleculesto favor crystallization[25,30]. Extrusion processing most

commonly combines the effect of high shear and high

temperature thus favoring starch granule breakage,

destruction and consequentgelatinizationwith the pro-ductionofhighlyamorphousandaccessiblestarch assem-blies[9,31,32].However,theextrusionprocessmightbe optimized to favor incorporation of lipids into swollen amylose(amylose–lipidcomplexes),formationofstarch– proteininteractions,de-branchingof amylopectin mole-cules producing straight chains that are more likely to retrograde [24,25,33]. All these phenomena favor the

formation of non-accessible structures and delay the

speed ofstarch degradation.

Summarizing, in order to reduce starch digestibility,

processing conditionsshouldbecarefully optimizedto: 1) Preserveasmuchaspossiblegranular/crystalline

struc-tures and/or favor the formation of

retrograded-crystallinestructures

2) Limitmobilityof gelatinized-amorphousmatrix

3) Preserve/build barrierstosurroundgelatinizedstarch

Preserving

the

native

structure

of

plant

tissue

in

starch-rich

foods

Instarchyfoods,thepresenceofintactcellwallsprevents thecompleteswellingofstarchgranulesduring

gelatini-zation and restricts their interaction with digestive

enzymes. Besides the cell wall, starch granules are

embedded in a tightlypacked cytoplasmic matrix, also

hindering enzymes’ diffusion, and restricting complete

starchgranuleswellingduringgelatinizationduetosteric hindranceandotherlimitingeffects(i.e.restrictedwater availability) [34].

Toleverageontheeffectivenessofnativestructurewith

the goal to prevent/delay starch digestion, mechanical

processes, and especially milling, must be carefully

designed. Millingof grains intoflour disruptscellwalls andhenceincreases accessibilityofstarchbyamylolytic enzymes, especiallywhentheflouris processedin food

using conditions favoring starch gelatinization. It is

knownthatglycaemicresponsesofwholemealandwhite

breadarecomparablebecausebothflourshaveundergone structural disintegrationduring milling.Conversely, the

glycaemic responses decreased linearly with increasing

proportionofwholeandintactgrainspresentinwheator barley bread [35]. The presence of higher portions of intactcellsincoarseflour(averageparticlesize:705mm) reducedtheinvitrostarchdigestionrateascomparedto fineflourandflour(averageparticlesize:85and330mm, respectively) with lower or negligible content of intact

cells [36]. However, when cell wall structure was

degradedbyxylanase,therateofdigestionincreasedalso in coarse flour,confirming thatintactwheat endosperm cellwallsposeaphysicalbarriertoamylasediffusioninto thecells[36].

Inevaluatingstarch digestibility, thebotanicaloriginof starchy foods isalso an important featureto be

consid-ered. When in vitro amylolysis of hydrothermally

pro-cessedchickpeaanddurumwheatwithdifferentparticle sizeswasstudied,durumwheatcellwallsareless effec-tive as enzyme barriers than chickpea cell walls [37].

Moreover, a different gelatinization behavior was

reportedforthesetwoplantspecies:theextentof gelati-nizationwasinverselyrelatedtoparticlesizeandstrongly correlatedtostarchdigestibilityinchickpeabutitwasnot in durum wheat [38]. Thickand mechanically resistant natureofthecotyledoncellwallsinlegumesmayrestrict

the access of digestive enzymes and also prevent the

complete swelling of starch granules during gelatiniza-tion. The thin cellwalls of cereals endosperm are less efficientinlimitingstarchdigestion.However,the poros-ityandpermeabilityofthewallsplayalsoapivotalrolein

theextenttowhichdigestiveenzymesenterand

hydro-lyzedproductsdiffuseoutofcells.Lietal. [39]showed redkidneybeanshavealessporousstructurecomparedto potatocells,suggestingthatthisfeaturecouldalsoexplain thelowstarch digestibilityinbeans.

Depending upon the processing conditions that plant

foods undergoand theirtissue characteristics (e.g. cell– celladhesionstrength),cellscaneitherseparatealongthe middle lamella or rupture across cell walls [40]. High pressure processing of legume cotyledons fractures cell walls and liberates nutrients enclosedwithin cells [41].

When domestic cooking is applied, cell walls appear

intact and retain their morphology even in rice where

most of the starch granules are disrupted and digested

[42]. However, thermal processing modifies cell wall

architecture(e.g.swelling,increasesolubilityand poros-ity,etc.).Theeffectivenessofcellwallsinlimitingstarch digestionchangesasprocessingconditionsaremodified. Pallaresetal.[43]foundthatthecotyledoncellsisolated

fromcommonbeans hadsimilar microstructural

proper-ties and starch gelatinization degree and retained their

different times (between 30 and 180min). However, a

higher diffusion of fluorescently labelled pancreatic

a-amylase inside the cells was shown with increasing

processingtime.Solubilizationofpectinandother poly-mers,probablyfromthepectin,celluloseand hemicellu-losenetwork,couldhaveledtodifferentdegreesof cell

wall permeability to a-amylase. However, crosslinking

betweenmatrixpolymersinthecellwallmayimpartwall strengththatresistssolubilization.Potatovarietieswitha

high amount of rhamnogalacturonan galactans, which

interact strongly with cellulose, in cellwall have lower pectinsolubilizationduringcookingandaninvitrostarch digestibilitythancommonpotatoes[44].

Different combinations of processing variables could

generate differentmicrostructures with different starch digestibility. Pallares et al. [45] generated different microstructure applying a traditional thermal treatment (95C,0.1MPa)andtwoalternativetreatmentsincluding

high hydrostatic pressure at room temperature (25C,

600MPa) and at high temperature (95C, 600MPa) to

common beans. In both treatments involving high

temperature,theloweststarchdigestibilitywasobserved

in samples mostly characterized by the presence of

cellclusterscompared tosamplesobtainedbythesame

processing technique but exhibiting a different

microstructure(individualcells).Inhighhydrostatic pres-sure-treatedsamplesatroom temperature,starch gelati-nizationhappenedtoalowextentduetotheabsenceof

high temperature. Therefore, although starch granules

werenothindered by physical barriers, theirhydrolysis

was reduced due to the preservation of native

organization.

Tosum up,foodsproducedbyusingmilled grainswith

large particle size would represent a useful strategy to reducetheirstarchdigestibility.‘Mild’millingcanproduce large clusters of intact cells in which the diffusion of digestiveenzymes to the core of theparticles is slower comparedto small particles [46]. Shorttime processing, whichaffectslessthepermeabilityofcell wallsand pro-duceslargecellclusters,isalsodesiredtolimitthestarch digestibility.Finally, thedesign ofbiomimeticfood sys-tems, for example, starch-entrapped microspheres fabri-catedbyentrapmentofstarchgranulesincalcium-induced gelnetworkofpectinandalginate,couldbethenearfuture inthedesignofslowlydigestiblestarchfoods[40].

Modulating

Maillard

reaction

in

starch-rich

foods

TheMaillardReaction(MR)typicallyoccurswhen

star-chy foods are roasted, baked or fried. At afirst glance,

becauseoftheextensivethermaltreatments,MR

devel-opmentcanbeassociatedwithstarchgelatinization,and sowithfoodhavingahighstarchdigestibility.However, thisisnotcompletelycorrect:MRdevelopsfasterinfood processedatlowwateractivity,aconditionthatalsofavors limitedstarchgelatinizationandformationofslow digest-ible starch [47]. In other words, two opposite effects

related to low water activity take place in food: MR

Figure2 •Preserve granular/crystalline structures •Promote starch retrogradation •Limit mobility of amporphous matrix • Preserve intact cell wall • Use large particle size flours • Favor mashing over milling • Strength protein network around granules • Convert starch in melanoidins • Favor roasting and dry baking over boiling

Current Opinion in Food Science

developmentandinhibitionofstarchgelatinization.The

moststraightforwardexampleto observethis

phenome-nonisabreadloaf:inthecrumb,theabundanceofwater

promotes starch gelatinizationwith minimalMR

devel-opment. In the crust, the formation of the brown MR

polymers,themelanoidins,isaccompaniedbyareduced

starch digestibility.This isduetothereactionofstarch withtheaminogroupavailableonproteinleadingtothe

formation of abrownheterogeneous polymer knownas

melanoidins [48]. There are few papers dealing with

starch-containing cereal melanoidins: these molecules

are difficult to extract, poorly digestible and a good

substrate for humanmicrobiota [49].The possibilityto

use arangeofbaking conditionsmodulating time,

tem-perature and moisture provides many opportunities to

design breadhavingreduced starchdigestibility[50].In

general formulation with different ingredients can be

usedtomodifythepropertiesofthefoodmatrix surround-ingthestarch granulestomodulatetheirdegradation

In the same vein, also pasta drying conditions can be

modulated to change starch digestibility: when a low

temperature is used for drying (common in artisanal

processing)noMRproductsareformed,andtheprotein

matrixisquiteopen:whencookedthestarchgranulescan easilygelatinizeandbecomingfullydigestible.However,

whenmore severedryingconditionsareusedas it

hap-pensinindustrialdryingofpasta,thehightemperatureat

low water activity promotes the formation of a strong

protein network reinforced by MR products covalently

bound to different gluten protein chains (crosslinking) [51].Starchgranulesarestiffedwithinthematrixanddo notcompletelygelatinizeevenduringcookinginexcess boilingwater[52].Asimilarapproachcanalsobepursued in extrudedproducts like breakfast cereals:Singh et al.

reported thatseverethermaltreatment and presenceof

reducingsugarreducesthenutritionalqualityofthefinal productsbypreventingstarchdigestion[53].Now look-ingfromtheoppositestandpointofreducingthecalorie uptakefromthestarch-richfoods,wecanmakeagooduse oftheextrusionprocesstopreventthestarch gelatiniza-tion and to trap the starch granules in a matrix rich in

indigestibleMRproducts.

Conclusion

Fightingobesityisachallengethatfooddesignersmust tackleinapragmaticwayusingallthepossibilitiesoffered

bynewingredientsandadvancedprocessingtechniques.

We must look attheproduct from theconsumers’

per-spectivesconsideringpsychologicalandhedonisticaspect

taking in mind that long-term dietary behaviors are in

most of thecases driven bylikingbefore than healthy,

convenience and sustainability considerations. This is

particularly truefor low educated andlow-income

con-sumerswhofindinstarch-richfoodsthebestsolutionto fulfill theireating preferenceataffordableprize.

Starchdigestionprovidesourbodywithalargemoietyof thedailycalorieintake:targetingthisphysiological pro-cesshasthepotentialtoimpactonthenegativemetabolic

consequences that an excessive occurrence of glucose

load has on human health. Recently a great interest

was devoted to theuse of amylaseinhibitorsespecially

polyphenols whichact in multiplewaysdelaying

diges-tive enzyme activity (see for review Lijun et al. [54]). Details ofthis approach arenot describedin this paper butitisrelevanttomentionthatpolyphenolsinteraction

with amylase canbe also modulated byprocessing and

formulationaddinganotherelementofvariability tothe wholepicture.

Dogmatic classificationsoffoodintogoodandbad

cate-gories, such as those proposed by NOVA, YUKA and

SIGAandalsotheNUTRISCOREsystem,donotserve

the purpose of reducingthe obesityof vulnerable

con-sumers and impairing theinnovation atfood industries

includingthedesignof healthierfoods[55,56].

The differentfood designapproacheshighlightedin this

paper and the mainrecommendation aresummarized in

Figure2.Thefinalmessageisthatacombinationof formu-lation and processing strategies can be very effective in achievingthe objectiveofdesigningstarchyfoodshaving reduced/delayed digestibility.The future challenge isto obtainthisgoalmatchingconsumers’sensoryexpectation withthepublichealthneeds.

Funding

This research did not receive any specific grant from

funding agencies in thepublic, commercial, or not-for-profitsectors.

Conflict

of

interest

statement

Nothingdeclared.

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