Rev Colomb Cienc Pecu 2016; 29:77-90

Revista Colombiana de Ciencias Pecuarias

Original articles

77

Literature Review

Starch in ruminant diets: a review¤

Almidones en la alimentación de rumiantes: revisión de literatura

Amido na alimentação dos ruminantes: revisão de literatura

Luis M Gómez1,2,3*, MVZ, MSc, (c)Dr. Sc; Sandra L Posada2, Zoot, MSc, Dr. Sc; Martha Olivera3, MV, Dr. Sc.

1Departamento de Investigación y Desarrollo, Grupo Nutri-Solla, Solla S.A., AA 1272, Itagui, Colombia.

2GRICA Research Group, Facultad de Ciencias Agrarias, Universidad de Antioquia, AA 1226, Medellín, Colombia.

3BIOGENESIS Research Group, Facultad de Ciencias Agrarias, Universidad de Antioquia, AA 1226, Medellín, Colombia.

(Received: April 15, 2015; accepted: November 11, 2015)

doi: 10.17533/udea.rccp.v29n2a01

¤ Tocitethisarticle:GómezLM,PosadaSL,OliveraM.Starchinruminantdiets:areview.RevColombCiencPecu2016;29:77-90.* Correspondingauthor:LuisMGómez.DirectorofResearchandDevelopment,SollaS.A.Company.Carrera42No.33-80Itagui,Colombia.Tel+574

4448411.E-mail:lmgomezo@solla.com

Summary

Background:starchisanimportantenergysourceforruminantsnutrition.Thiscarbohydrateisoftenusedtoimproverumenfermentation,optimizingdigestionofstructuralcarbohydratesandincreasingproteinflowtothesmallintestine.Microbialanddigestiveenzymesareinvolvedinstarchdigestion,generatingproductsthatcanpositivelyornegativelyaffectanimalperformanceandhealth,dependingonthestarchcontentsofthediet. Objective: todescribethebasiccharacteristicsofstarches,thefactorsaffectingitsnutritionalavailability,anditseffectsinruminants.Conclusion:anumberoffactorsaffectstarchdigestibility,includinggranulesize,amylose/amylopectinratio,proportionoffarinaceousandvitreousendosperm,presenceofstarch-lipidandstarch-proteincomplexes,andphysical-chemicalprocessingofthefeed.Ingestionoflargeamountsofstarchcantriggerruminalacidosis.However,itsrationaluseinthediethaspositiveeffectsonmethaneemissions,andinmilkyieldandcomposition.

Keywords: acidosis, amylopectin, amylose, digestibility, lactation, methanogenesis.

Resumen

Antecedentes: elalmidónesunimportanterecursoenergéticoparalaalimentaciónderumiantes.Estecarbohidratoesfrecuentementeempleadoparaelmejoramientodelosparámetrosdefermentaciónruminal,loqueoptimizaelaprovechamientodeloscarbohidratosestructuraleseincrementaelflujodeproteínaalintestinodelgado.Ensudigestiónparticipanenzimasmicrobianasydigestivas,lascualesgenerandiferentes

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productosqueimpactanpositivaonegativamenteeldesempeñoproductivoylasaluddelanimal,dependiendodel nivel de almidón en la dieta. Objetivo: describirlascaracterísticasbásicasdelosalmidones,losfactoresqueafectansudisponibilidadnutricionalylosefectosdesuutilizaciónenlaalimentacióndelosrumiantes.Conclusión:existeunsinnúmerodefactoresqueafectanladigestibilidaddelalmidón,entreellos,eltamañodelgránulo,larelaciónamilosa/amilopéctina,laproporcióndeendospermofarináceoyvítreo,lapresenciadecomplejosconlípidosyproteínas,ysuprocesamientofísico-químico.Laingestióndegrandescantidadesdealmidónpuededesencadenaracidosisruminal;noobstante,suempleoracionalenladietadelosrumiantestieneefectospositivossobrelaemisióndemetano,ylaproducciónycalidaddelaleche.

Palabras clave: acidosis, amilopectina, amilosa, digestibilidad, lactancia, metanogénesis.

Resumo

Antecedentes: oamidoéumaimportantefontedeenergianaalimentaçãodosruminantes.Estecarboidratoégeralmenteutilizadoparamelhorarosparâmetrosde fermentaçãonorúmen,oqueotimizaautilizaçãodoscarboidratosestruturaiseaumentaofluxodeproteínaparaointestinodelgadodoanimal.Nasuadigestãoestãoenvolvidasenzimasdigestivasemicrobianas, asquaisgeramdiferentesprodutosque impactampositivaounegativamenteodesempenhoprodutivoeasaúdedoanimaldependendodoníveldeamidonadieta.Objetivo: descreverascaracterísticasbásicasdoamido,factoresqueafectamasuadisponibilidadenutricionaleosefeitosdasuautilizaçãonaalimentaçãoderuminantes.Conclusão: diversosfatoresafetamadigestibilidadedoamido,incluindootamanhodogrânulo,arelaçãoamilose/amilopectina,aproporçãodeendospermafarináceoevítreo,aformaçãodecomplexoscomlipídeoseproteínaseoseuprocessamentofísico-químico.Aingestãodegrandesquantidadesdeamidopodeprovocaracidoseruminal,noentanto,asuautilizaçãoracionalnaalimentaçãoderuminantestemefeitospositivossobreasemissõesdemetano,aproduçãodeleiteeasuaqualidadecomposicional.

Palavras chave:acidose, amilopectina, amilose, digestibilidade, lactação, metanogênese.

Introduction

Starch–thelargestreservoirofplantpolysaccharides-playsanimportantroleingerminationandgrowth,anditssynthesisissecondonlytothatofcellulose.Starchisthemainenergycomponentusedinruminantfeedsdue to its availability (Ortega andMendoza,2003). It is often included in the diet to improveruminal fermentation, allowing for a better use ofstructuralcarbohydratesandtoincreaseproteinflowtothesmallintestine(Huntingtonet al.,2006).Starchsourcesareexpensive,sotheymustbeusedwiselytobecost-effective.Itisimportanttounderstandthestructural characteristics of starch, its ruminal andpost-ruminaldigestion and the factors affecting itsdigestibility in order to improve performance andprofit of livestock systems.This reviewdescribesstarch,thefactorsaffectingitsnutritionalavailability,anditseffectsinruminantfeedingandnutrition.

Description of starch

Composition

Starches aremainly α-glucans composed oftwo types ofmolecules: amylose and amylopectin

(SantanaandMeireles,2014;Table1).AmyloseisalinearD-glucosepolymercontainingabout99%α-1,4links(ParkerandRing,2001).Amylopectin,whichhas95%α-1,4linksand5%α-1,6links(Stevneboet al.,2006),isthemostabundantcomponentofstarches(Figure 1).On the other hand, amylose content instarchusuallyfluctuatesfrom200to300g/Kg.Somestarch-richfeedssuchaswaxycerealsusuallycontainnegligibleamountsofamylose,whilehigh-amylosesourcesmaycontainupto700gamylose/Kg.Cerealssuchaswheat,maize,barley,andricecancontainawaxygenederivedfromnaturalmutationsofgenesencoding granule bound starch synthase,which isrequiredforamylosesynthesis(Svihuset al.,2005).

Structure

Starchgranulesareformedbyconcentricallygrowinglayersalternatingsemi-crystallineandamorphousfilms(Figure1).Thesemi-crystallineregionismoreabundantinamylopectinand ismore impervious toenzymaticattackbecauseofitsresistancetoentryofwater.Theamorphous region is rich inamyloseandhas lowerdensitythanthecrystallinearea,whichfacilitateswaterflowandenzymeattack;however, it is abundant inhydrogenbonds(Perezet al., 2009).

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Table 1. Properties of starch components.

Characteristic ComponentAmylose Amylopectin

General structure Linear Branched

Branch sites Nonea 1 per 20 to 25 glucose units

Polymerization degreeb

Molecular weight~1.000

1 x 105-1 x 106 g/mol~10.000-100.000

1 x 107-1 x 109 g/mol

Stability in solution Low Higha There is a type of branched amylose with 1 or 2 α-1,6 links per molecule. b Number of glucose residues per molecule.Adapted from Parker and Ring, 2001.

Figure 1. (A) Structure of starch granules, represented by organized laminar forms. Amorphous rings (composed mainly of amylose) separate layers in the semi-crystalline regions (composed primarily of amylopectin). Modified from Perez et al., 2009. (B) Amylopectin structure according with the cluster model by Myers et al., 2000. Glucan chains are depicted by solid lines while intersections between them indicate branch linkages. The dotted lines show the limit of amylopectin side chain clusters with unbranched chains associated in tightly packed double helices. a) depicts the amorphous areas separating amylopectin side chain clusters.

A

B

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Structural alterations

Gelatinization. It is the permanent alterationof the granule structure by breaking its hydrogenbonds.Starch absorbswater duringgelatinization,theexpansionbreaksthehydrogenbondsreleasingsomeoftheamylosebyleaching,thusbirefringenceis reduced and starch becomes more solubleand exposed to enzyme activity (Rooney andPflugfelder,1986).Inexcessofwater,moststarchesgelatinise at temperatures higher than 80 °C.Thegelatinisationtemperatureishigherforsmallstarchgranules.Amylose-rich cereals aremore resistanttogelatinisationthancerealswithnormalandhighamylopectin levels (Svihus et al., 2005).Table 2shows gelatinization values for several foods andprocessingmethods.The degree of gelatinizationis higher for extruded vs. pelleted food since thetemperatureusedintheprocessishigher(upto250°Cvs.60-95°C;Caballero,2010).

Table 2. Starch gelatinization under several processing methods in various feeds.

Food Gelatinization (%)1 Processing

Corn 17.06 Unprocessed

Sorghum 12.47 Unprocessed

Yucca 7.59 Unprocessed

Concentrate 1 32.49 Pelleting

Concentrate 2 32.55 Pelleting

Concentrate 3 31.92 Pelleting

Corn 79. 3 Extruded

1Assessed by an enzymatic method (Medel et al., 1999).

Retrogradation. It is defined as the reversiblereturnofasolubilized,dispersedoramorphousstatetoacrystallineorinsolubleform,whichlimitsstarchdigestibility.Amylose is themain component thatfacilitatesretrogradation(Biliaderis,2009).

Sources of starch

Cereal grains and roots

Cerealgrainsareamajor sourceof starchusedinanimalfeeds.Cerealsarecomposedofpericarp,endosperm and germ (Figure 2). The pericarp

comprises3to8%ofthekernelweight,althoughitcanbeupto25%inoats(Everset al.,1999).It ismostlycomposed(90%)ofhighlylignifiedfiberandthestarchcontentislessthan10%(Liet al.,2007),thuspericarpdigestibilitydoesnotexceed40%(VanBarneveld,1999).

Figure 2.Cornkernelcomposition.AdaptedfromEckhoffandWatson(2009).

Theendospermrepresentsbetween60and90%ofthegrain.Itisthemorphologicalstructurecontainingthe starch. It also contains proteins, phospholipidsandash,butlittleneutraldetergentfiber(NDF)andphosphorus (P; Eckhoff andWatson, 2009).Theendospermlayers,fromtheoutsidein,arealeurone,peripheralendosperm,horny(orvitreous)andfloury.Boththeperipheralandthehornyendospermhavestarch granules surrounded by amatrix abundantin hydrophobic proteins called prolamines andnon-starch polysaccharides (PNAs; β-glucans,arabinoxylans, and pectins),which are relativelyimpermeabletowaterandenzymaticactivity(ZeoulaandCaldasNeto,2001;Giubertiet al.,2014).Grainsexhibitinghighproportionofperipheralandhornyendospermarecalledvitreousorhorny,whilethoseabundantinflouryendospermarecalledopaqueorsoft(ZeoulaandCaldasNeto,2001).

Non-conventional sources

Starchrepresentsanimportantfractioninmanycrops.Mostcereals(i.e.corn,wheat, rice,oat,andbarley) containbetween60 and80%starch,whilelegumes (chickpea, bean, pea) contain from25 to

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50%, tubers (potato, cassava, cocoyam,arrowroot)from 60 to 90%, and some green fruit (banana,mango) contain asmuch as 70% (Santana andMeireles,2014).Asincereals,thelargestproportionofstarchcorrespondstoamylopectinandthesmallestto amylose (17-30%;Hu et al., 2010).Amyloserepresents14to19%ofstarchincassava,between2and22%inpotato,andapproximately37%inplantain(Knowleset al.,2012).Amylopectininstarchfrompotatoislessbranchedcomparedtocereals(Alvaniet al.,2011).Itisalsohighlyexpandable(VasanthanandBhatty,1996)andgelatinizesat relatively lowtemperature (between64.4and69.9°C)comparedtootherstarches(Hernandez-Medinaet al.,2008).

Table3showsamyloseandamylopectinconcentrationindifferentstarchyfoodsandconcentratesfedtodairycattle.Differencesinamylose/amylopectinratioaffecttherateofruminalorintestinaldigestion.Digestionrateofamylopectinisusuallyhigherthanthatofamylose(Knowleset al.,2012).

Table 3. Amylose and amylopectin content in various feeds.

Source Amylose (%) Amylopectin (%)

Corn 29.24 70.76

Sorghum 29.55 70.45

Yucca 19.84 80.16

Concentrate 1 (C1)* 21.17 78.83

Concentrate 2 (C2) 22.22 77.78

Concentrate 3 (C3) 20.25 79.75

Concentrate 4 (C4) 24.89 75.10

*Isoenergetic and isoproteic concentrates (C) for dairy cattle formulated with four carbohydrate sources: corn (C1), sorghum (C2), yucca (C3), citrus pulp (C4). Assessed using the method described by Gibson et al. (1997).

Ruminal and post-ruminal digestion of starch

Once it reaches the rumen, starch is degradedmainly by amylolytic bacteria and by fungi andprotozoatoalesserextent(Huntington,1997).Theα-1-4andα-1-6endoandexoamylasesproducedbyrumenmicroorganismshavetheabilitytohydrolyzeamylose and amylopectin glycosidic linkages,releasingdifferentoligosaccharides(Table4).

Thepost-ruminal process of starch degradationbeginswith pancreatic α-amylase secretion,whichhydrolyzes amylose and amylopectin into dextrinsandlinearoligosaccharideswithtwotothreeglucoseunits.The process is completed by the action ofoligosaccharidases(maltaseandisomaltase)secretedintheintestinalmembrane(OrtegaandMendoza,2003).

Inruminants, thesiteofstarchdigestionaffectsthesubstratesabsorbed.Ruminaldigestiongeneratesvolatilefattyacids(VFA)forabsorptionandprovidesenergyformicrobialproteinsynthesis(HuhtanenandSveinbjörnsson,2006). Decreasedrumendigestibilityofstarchisdesirabletopreventfromacidosisandtoincreasethesupplyofglycogenicsubstrates(Svihuset al.,2005).Starchdigestioninthesmallintestineimpliesgreater energetic efficiencycomparedwithruminaldigestionduetoreducedmethaneproductionand fermentationheat losses andhigher efficiencyofmetabolisable energy utilisation (Huhtanen andSveinbjörnsson,2006).Nevertheless, the increasedenergyefficiencyfromhigherstarchdigestioninthesmall intestine is offset by the increase in hindgutfermentation,becauseonlyVFAareabsorbedfromthehindgutwhereasmicrobialmatterisexcretedinfeces.Adecreaseinruminalstarchdigestionisnotassociatedwith an increase in its small intestinal

Table 4. Enzymes involved in starch hydrolysis.

Enzyme Link End product

Phosphorylase α -1-4 glycosyl Glucose 1 phosphate

Alpha-amylase α -1-4 glycosyl Linear and branched oligosaccharides

Beta-amylase α -1-4 glycosyl Maltose and limit dextrins

Amyloglucosidase α -1-4 glycosyl and α -1-6 glycosyl Glucose

Isoamylase α -1-6 glycosyl Lineal chains of α -1-4 glucans

Pullulanase α -1-6 glycosyl Lineal chains of α -1-4 glucans

Adapted from Tester et al., 2004.

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digestion,butitisassociatedwithhigherhindgutandlowertotaltractdigestibility(Larsenet al.,2009).

Forthisreason,rumenisconsideredtheprimarysite of starchdigestion.Ruminal digestionusuallyaccountsfor75to80%oftheintake,andabout35to60%of thestarchenteringthesmall intestine isdegraded.About35to50%ofthestarchthatescapesdigestion in the small intestine is degraded in thehindgut(Harson,2009).Accordingtoameta-analysisbyMoharreryet al.(2014),ruminalstarchdigestibilityvariesgreatly(from224to942g/Kg).Theauthorsalsonotedthatstarchconsumptionadverselyaffectedruminalstarchdigestibility,obtaininganegativeslopeof1.4%perKgincreaseindailystarchintake.Table5 presents the content and ruminal digestibility ofvarious starch sources used in livestock.

Table 5. Starch content and ruminal digestibility of several starch sources commonly used as feed supplements in dairy cattle.

Grain Starch (%) Rumen digestibility (%)a

Corn1,2 76.0 72 - 89.9

Sorghum1,2 71.3 60 - 78.4

Wheat1,2 70.3 88.3 - 88.1

Barley1,2 64.3 80.7 - 84.6

Oats1,2 58.1 92.7 - 94.0

Yucca3 80.0 91.0

a Variability is explained by grain treatment (grinding, rolling, flaking). 1 Herrera-Saldana et al., 1990. 2Huntington, 1997. 3Vearsilp and Mikled, 2001.

Factors affecting starch digestibility

Granule size

Thisisalimitingfactorinstarchdigestionbecausetherelationshipbetweenstarchvolumeandsurfacearea,andthussubstrate-enzymecontact,decreasesasgranulesizeincreases(Sviluset al.,2005).Cerealswithsmallgranules,suchasoatsandrice,aremoredigestiblethancorn,wheatandpotato,whichhavelonggranules(Bednaret al.,2001;Sviluset al.,2005).

Amylose/amylopectin ratio

Several studies have shown that amylose/amylopectinratioisnegativelycorrelatedwithstarch

digestion(Bednaret al.,2001).Amyloseisinsertedintoamylopectinmoleculesincreasingtheamountofhydrogenbondswithin the starchmolecule,whichnegatively impacts the ability of expansion andenzymeactivity(Caldas-Netoet al., 2000).Likewise,starchgranuleswithhighamylosecontentaremorepronetoretrogradation(Sviluset al.,2005).

Floury versus vitreous endosperm

Severalresearchers(Correaet al.,2002;Ngonyamo-Majeeet al.,2008)havereportedaninverserelationshipbetweenstarchdigestibilityandvitreousness.Allenet al.(2008),studiedruminalandduodenal-fistulatedcows using cornwith vitreous endosperm contentvaryingbetween25and66%.Theyfoundthatfeedingcornwith66%ofvitreousendospermreducedruminaldigestionin19.1%andoveralldigestionin7.1%.

Starch-lipid complexes

Quantitatively, lipids are themajor non-starchcompoundsinstarchgranulesandcanbefoundasfreefattyacids(mostlypalmiticandlinoleicacid)and lysophospholipids (Svihus et al., 2005). Incereal grains, a portion of amylose has insolublestarch-lipidcomplexes,whichformhelicalstructuresthat provide greater adhesion betweenmolecules,dininish starch swelling (Vasanthan andBhatty, 1996), decrease their solubility (Rooney andPflugfelder,1986)andreducetherateofenzymaticdigestion(Croweet al., 2000).Cassavaandpotatostarch contain a smaller percentage of lipidscomparedwith cereal starch (Zeoula andCaldasNeto,2001;Alvaniet al.,2011).

Starch-protein complexes

The proteinaceousmatrix surrounding starchgranulesaffectsstarchdigestibility.Digestibilityisnegativelyassociatedwiththepresenceofprolamins.Prolaminsarestorageproteinsthatreceiveadifferentnameforeachcereal,namelyzein(corn),kafirins(sorghum), gliadin (wheat), hordeins (barley),secalins(rice),andavenines(oats).Usually,wheat,oats, rice and barley have fewer prolamins thancornandsorghum(Momanyet al.,2006;Giubertiet al.,2014).

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Zeinsaccountfor50to60%oftheproteininthewholegrainandarelocatedattheperipheryofthecell.Flouryendospermislowinzeincomparedwithvitreous endosperm (Giuberti et al., 2014). Zeinsarenotsolubleintherumenenvironment(Lawton,2002).Starchdigestionrequiresthatrumenbacteriadegradezeinsfirstviaproteolysis,beforestartingtheamylolyticactivity(Cotta,1998).

Processing of cereal grains

Grain processing using temperature, humidityandpressurefacilitatebindingofbacteriatostarchgranules, increasing itsdigestibility (Huntingtonet al., 2006).Commonprocessing includes grinding,pelleting, dry rolling, steam rolling (addition ofwater before rolling), and steamflaking.All theseprocesses aim to break grain barriers such as thepericarp and the protein-starchmatrix, allowingaccessofmicroorganismstostarchgranules.Theseprocessesalsoreducetheparticlesize,andincreasesurfaceareaandmicrobialcolonization(Giubertiet al., 2014).The response to processingvarieswithdifferentgrains,withsorghum>corn>oats=barley>wheat(Huntingtonet al.,2006).

Gelatinizationofstarchmakesitmorewater-solubleanddigestible.AccordingtoHuntington(1997),steamflakingofcornimprovesruminal,post-ruminalandtotaltractdigestibilitycomparedwithdryrolling(85vs.70%,92vs.69%,and99vs.90%,respectively).AccordingtoSveinbjörnssonet al.(2007),heattreatmentincreasesstarchdegradationduring8hofin vitro incubation,asfollows:0.155vs.0.870forpurepotatostarch,0.491vs.0.815forpeas,0.686vs.0.913forbarley,and0.351vs.0.498formaize.

Only a fraction of starch is gelatinazed duringsteamconditioningandpelletingoffeeds(from10to200gstarch/Kg).Theexpanderprocessing,ontheotherhand,addsupto80gwater/Kgwhilethedietreachesahighpressureandtemperaturesabove100°C,thusresulting inbetween220and350gstarch/Kggelatinizedduring thisprocess.Theextrusionaddsevenmorewater(upto180gwater/Kg)andthedietissubjectedtoevenhighertemperatures(>110°C)underhighpressure,thusresultinginmorecompletegelatinisation anddisintegrationof starchgranules(Svihus et al.,2005).ThiswasevidencedbyOffner

et al.(2003),whoreported0.607,0.663,0.743,0.746,0.819, 0.830, and 0.867 effective degradabilitiesforuntreated,cracked,ground,pelleted,expanded,steamflakedandextrudedcorn,respectively(passagerate0.04h-1).Graintypealsoinfluencestheresults.Steamflakingofcorneliminatedtheadverseeffectsofvitreousendospermandprotein-starchmatrixondigestibilityincomparisonwithdryrolling.Thiswascontrary to the results obtained for barley, a grainwithahighlydigestibleprotein-starchmatrix,wherenodifferencewasobservedbetweenbothtreatments(Engstromet al.,1992).

Starch source

The highest effective degradability of starchin cereal grainswas obtained for oats,wheat andbarley, being lower for corn and sorghum.Cornand especially sorghum have a high proportionof peripheral and horny endosperm resulting inincreased resistance tomicrobial activity (RooneyandPflugfelder,1986),unlikewheatandoats,whichhave higher proportion of floury endosperm. Inaddition, corn and sorghumhave a denser proteinmatrix(Kotarskiet al.,1992).Thein vitro experimentbyLanzaset al.(2007)measuredfractionalgasrates,as ameasure of starch digestion (Huhtanen andSveinbjörnsson,2006),reporting0.26,0.24,0.15,and0.06h-1ratesforwheat,barley,cornandsorghum,respectively(p<0.001).

Cassavahashighereffectivedegradabilitythancornandsorghumduetoitslackofpericarp,proteinmatrix,hornyandperipheralendosperm;aswellaslowproportionoflipids,lackofassociationsbetweenstarchandprotein,lessamylose,moreamylopectin,lesshydrogenbonding,andgreaterswellingwhensubjected to chemical processes. Cassava starchis composed exclusively of amylopectin in thecrystalline region and amylose in the amorphousregion, which prevents excessive formation ofhydrogenbondswithamylopectin,allowingamyloseto be readily leached.This is contrary to cereals,whichhaveamyloseinthecrystallineregion(ZeoulaandCaldasNeto,2001).Effectivedegradabilityofcorn, sorghumandcassava, reportedbyOffneret al. (2003),was0.597,0.603y0.802,respectively(passagerate0.06h-1).

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Physiological restrictions of the small intestine

Starch digestibility in the small intestine islimited.Asdigestaflowincreases,starchdigestibilitydecreases (Huntington et al., 2006). Factors thatlimitstarchdigestibility includecontrolledglucoseabsorption,deficientenzymeaccessibility tostarchgranules,alterationsinruminalandintestinalpH,andlackofsynchronybetweenstarchflowthroughtheintestineandamylasesecretion(Owenset al.,1986).

Starchdigestionefficiencyinthesmallintestinevariesbetweensources.Tothiet al.(2003)reportedhigher digestibility for barley starch in the smallintestine comparedwith cornstarch, resulting inhigher small intestine absorption in termsof g/Kgstarchingested.

Starch and ruminal acidosis

Starchfermentationincreasesvolatilefattyacids(VFA) and lactate production,which can reduceruminal pH and kill cellulolyticmicroorganisms,leadingtodecreasedfiberdigestibilityanddrymatter(DM) intake.Additionally, it can causemetabolicdisorders such as acute and sub acute ruminalacidosis, rumenitis, laminitis, liver abscesses andpolyencephalomalacia(Plaizieret al.,2009).

The risk of ruminal acidosis increaseswhenstarchdigestionrate increases.This ratevarieswithgraintypeandprocessingandgenerallyoccursinthefollowingorder:wheat(32%h)>oat>barley(29%h)>potato(5%h)>corn(2%h)andsorghum(Callisonet al.,2001;Mosaviet al.,2012).Krauseet al.(2002)reportedlowerruminalpHinlactatingcowsfedhighmoisturecornvs.driedcorn.GulmezandTurkmen(2007) observed a decreaseof ruminal pH (<6) inlactatingcowswhencornwasreplacedbywheat.TheyalsoobservedlowpH(<5.8)over13continuoushourswhenwheatwastheonlysourceofstarch.

Cassavaisusedasareadilyfermentableenergysource for ruminants. It has ahigh rate andextentof ruminal degradation, as evidenced byKhampaandWanapat(2006)whocomparedcassavavs.cornsupplementationat1and2%of liveweight.Theyfound that 2% cassava supplementation lowered

ruminalpH(5.3vs.6.4)andcellulolyticbacteria(2.3vs.5.9x107).

Starch and methanogenesis

Ruminal digestion of fiber-rich diets increaseshydrogen and carbon dioxide production,whichare substrates for methanogenesis. Moreover,starch-rich diets change the bacterial ecology byfavoring propionic-acid producing bacteria overmethanogens (Bannink et al., 2006; Ellis et al., 2008).Propionicacidproductionfromdicarboxylicacids(aspartate,malate,fumarate)viathesuccinatepathway is thermodynamically more efficientthanmethanogenesis (Offner andSauvant, 2006).Moreover,rapidly-fermentingdietsreducemethaneproductionbydecreasingruminalpH,whichaffectsthegrowthofmethanogens,protozoa(Hooket al., 2011)andcellulolyticbacteria (Sunget al.,2007),andincreasespassagerate,whichreducesprotozoansand,thereby,interspecieshydrogentransfer(Kumaret al.,2013).

Agleet al. (2010) reported thatdietswithhigherproportionofnon-structuralcarbohydrates(52and72%)resultedinnumericallylowermethaneemissions(1.5vs.3.4g/hour,respectively),althoughresultsshowednodifferenceduetohighvariability.ArecentstudyingrazingHolsteinFriesiancowsfoundthatconcentratelevel (2,4,6, and8Kg/cow/day)hadno impactonmethane emissions (287, 273, 272, and277g/day,respectively).However,when itwasassociatedwithDMandenergyconsumption,methanedecreasedwithincreasinglevelsofconcentrate(gCH4/KgDM:20,19.3,17.7,and18.1;CH4-E/grossenergyintake:0.059,0.057,0.053,and0.054,respectively).Theydemonstratedthatconcentratesupplementationtograzingcowsincreasedmilkproductionanddecreasedmethaneemissionsperunitofmilkproduced(Jiaoet al.,2014).Aguerreet al.(2011)foundthatchangingforage:supplementratio(F/S)from68:32to47:53reducedmethaneemissionsfrom648to538g/cow/day.Pirondiniet al.(2015)evaluatedtheeffectofstarch(23.7and27.7%DM)onmethaneemissionsindairycows,findingloweremissionsforstarch-richdiets(415vs. 396 g/d, respectively). Finally,Hatew et al. (2015) investigated the effect of starch (270 vs.530g/KgconcentrateDM)andfermentationrate

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(fastvs.slow)indairycows.TheyfoundnodifferencesinmethaneproducedperKgoffat-correctedmilkandprotein,orperKgDMconsumed,orasafractionofthegrossenergyconsumed.However,thehighstarchdiet (46.9vs.43.1g/Kg)hadlessruminalmethaneperKgof fermentableorganicmatter (42.6vs.47.4g/Kg).Haleset al.(2012)evaluatedtheeffectofcornprocessing.They found that Jersey animals eatingsteamedcornflakesproducedlessmethanethanthoseeatingdryrolledcorn(58.77vs.74.31L/animal,11.65vs.14.06L/KgDMintake,2.47vs.3.04%ofgrossenergyconsumed,and3.30vs.4.18%ofdigestibleenergyconsumed).Thereductionwasexplainedbydifferences in ruminal fermentation, changing theplaceofdigestion(fromtherumentotheintestine),ordecreasedruminalpH.Scarceliteratureisavailableontheeffectofstarchsourceandprocessingonmethaneemissions.InastudyreportedbytheCCRP(2012)areductionofmethaneemissionsincowsfedgroundwheat(219gmethane/day,11.1gmethane/KgofDMconsumed)vs.groundcorn(424and19.5gmethane,respectively).

Thedifference inmethaneproductionper starchvs. celluloseunit doesnotdependon the chemicalcomposition,asbothcarbohydratesarehydrolyzedtoglucosebeforefermentation.Conversely,hemicellulosepolymerincludessugarswith5to6carbons,whichcouldlead tochanges in the fermentationprofile (differentproportionsofVFA)andmethaneemissions.Ratherthanthechemicalcomposition,thedifferencesinmethaneproduction fromstarch, celluloseandhemicelluloseappear tobea functionof themicrobial species thatdegrade each substrate. Fermentation patterns andmethaneproductionvaryasmicrobialspeciesadapttochanges indietarysubstratesandruminalconditions.Additionally, associative effects between nutrientsinfluencemethaneproduction,whichmeans that thisgascanbeestimatedforthedietandnotforindividualingredients(Knappet al.,2014).

Relationship between starch and milk composition and yield

Effect on milk yield and fat content

Milk yield response depends on the starchsource(Khorasaniet al.,2001)anditsdegradation

rate. Mosavi et al. (2012) comparedmilk yield inHolstein cows consumingwheat, barley,maize orpotatoes.They found a reducedmilk yield for thediet addedwith potatoes, and attributed it to itslower digestibility. Supplementationwith rapidlydegradablestarchesinrumen-suchasbarley,wheator cassava- increases yield but reducesmilk fat(Sutton, 1989). Poore et al. (1993) found amilkyieldincreaseof3.4Kg/dayand0.4%fatreductionwhenruminaldigestibilityincreasedfrom48to72%.Milkfatreductionisassociatedwithchangesinthefermentationprofile,causedbyarelativereductioninlipogenicvs.glycogenicprecursors(Reynoldset al., 1997).Rumenpropionateincreaseswhileacetateandbutyratedecreasewheningestionofrapidlydegradablestarchexceeds7Kg/day(Casperet al.,1990).Jurjanzet al.(1998)evaluatedstarchsourceandlevel(wheatorpotatopeels;<5,6,or>7.5Kg/d)onmilkyieldandcomposition.Highstarchconsumption frompotatopeels(>7.5Kg/day)leadtoslowerruminaldegradationandincreasedmilkfatcontent(+3.3g/Kg)comparedtowheat.Fedinloweramounts,thestarchsourcedidnotaffectmilkfatsynthesis.Thelowerrateofstarchdegradationcouldhavereleasedmorefatprecursors.Mosavi et al. (2012)alsoobservedslower ruminaldegradation for corn starch comparedwithwheat,barley or potato, aswell as increased acetate andbutyrateproductionalongwithhighermilkfat(3.43%vs.3.12,3.09,and3.13%,respectively).Contrarytothesefindings,Chanjulaet al.(2004)didnotobservedifferences inmilk production and compositionalqualitybyaddingcorn(lowdegradability)orcassava(highdegradability)at two inclusion levels (55vs.75%).

AccordingtoKennellyandGlimm(1998),milkfatisreducedduetheinhibitoryeffectofmethylmalonylCoA(synthesizedfrompropionicacid)onfattyacidsynthesisinthemammarygland.MethylmalonylCoAaccumulation competitively inhibitsmalonylCoA(VanSoest,1994).

Reynoldset al.(1997)associatedmilkfatdecreasewithincreasedlevelsofplasmaglucoseandinsulinin animals fed high amounts of the supplement.Insulinlowerslipolysisandpromoteslipogenesisinadiposetissue,reducingfattyacidsavailabilitytothemammarygland,thusdecreasingmilkfat.AccordingtoVanSoest (1994), lipogenesis in adipose tissue

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is insulin dependent,which is not the case for themammarygland.

Thereductioninmilkfatcanalsobeexplainedbyincreasedtrans-unsaturatedfattyacidsintherumen(Gaynoret al.,1995).Cerealgrainsarehighinlinoleicand oleic acid.A ruminal pHdecrease due to thedietcandisturbbiohydrogenationofunsaturated18carbonfattyacidsincreasingtransC18:1fattyacid(transisomersresultfromincompletemicrobialbio-hydrogenationoflinoleicacidintostearicacid).ItisknownthatruminalandmilkincreaseintransC18:1iscorrelatedwithlowmilkfatlevelsincowsfedhighgraindiets(Griinariet al.,1998).Corncontainsahighconcentrationof linoleic (C18:2) andoctadecanoicacid (trans C18:1),whichinhibitbiohydrogenationandreducelipogenesisinthemammarygland.

AccordingwithMontoyaet al.(2004),theoptimalcontent of nonstructural carbohydrates (NSC) formaximizingmilkyieldisbetween30and38%ofthediet.Those researchers supplemented cowswith 4Kgofacommercialconcentrateand0,6,and12Kgoffreshpotatoes,thusNSCaccountedfor7.2,12.4,and17.9%ofDMintake.Milkyieldwashigherforthepotato treatments (17.2vs. 15.8 liters/cow/day; p=0.004).Nevertheless,nodifferencewasobservedfortheinclusionof6vs.12Kgpotatoes,whichcouldbeassociatedwithalimitedabilitytousepotatoNSC.Theirstudyfoundnodifferencebetweentreatmentsforfatpercentageandproduction(p>0.05).Pimentelet al.(2006)alsoevaluatedcassavasupplementationonmilkyieldandcomposition.Theyreplaced0,25,50,and75%ofcornwithcassava,findingalineardecreaseof30and1.15g/dayinmilkyield(correctedfor3.5%fat)andfatproduction,respectively.Accordingtotheauthors,theviabilityandlevelofcornsubstitutionwithcassavawilldependonalowcostofsubstitutionthatcompensatesfortheexpecteddecreaseinproduction.

Dann et al. (2014) evaluated three starch levels(17.7, 21.0, and 24.6%) inHolstein cows usingincreasing levels of ground corn.They found thatsolids-correctedmilkyieldwasnot affectedby thediet, averaging 40.8Kg/d.They concluded thatstarchcontentdidnot affect rumen fermentationorperformance.Theirhigheststarchlevel(onaDMbasis)wasbetween23 to30%,which followswithin therecommendedrangeforlactatingcows(Grant,2005).

Delahoyet al.(2003)conductedtwoexperimentsassuming that supplements such as steam-flakedcorn(SFC)andnon-foragefiber(NFF)sourcesmayprovidebenefitsovercorn. In thefirst experiment,animalswereassignedtoacracked-corn(CC)ortoasteam-flakedcorn(SFC)supplement.Inthesecondexperiment,animalswereofferedgroundcorn(GC)ornoforagesourcesoffiber(NFF).Nodifferenceswereobservedinmilkyield(24.3and27.5Kg/dforexperiments1and2,respectively),explainedbyalackofdifferenceinnetenergyconsumptionforlactation,which exceeded the requirements (Experiment 1).Anotherfactorthatcouldexplaintheseresultsisthequalityofthepasture,whichdidnotreducethepH,atargettoimprovebyNFFinclusioninExperiment2.

Effect on the protein content

Dietsrichinnonstructuralcarbohydratesincreaseruminalammonianitrogenutilizationandmicrobialprotein synthesis (Svihuset al., 2005).Therefore,whendietaryenergyincreases,metabolizableproteinis also increased. Mosavi et al. (2012) evaluatedtheeffectoffourstarchsourcesonmilkproteininHolstein cows.While protein levels ofmilkweresimilar (3.03, 3.10, 3.14, and 3.04%) forwheat,barley, corn and potato supplements, respectively,milkproteindifferedinfavorofwheat,barleyandcorn,comparedtopotato(1.08,1.06,1.06,and0.98Kg/d,respectively; p=0.02).GozhoandMutsvangwa (2008)foundnodifferenceinmilkproteinforanimalsfeddietsbasedonwheat,barleyorcorn,buthighermilkproteinwasobserved fordietsbasedoncornvs. oats.On the contrary, other studies comparingslowversusfastruminaldegradingstarchesfoundnodifferencesinmilkprotein(Khorasaniet al.,2001;Silveira et al.,2007;Cabritaet al.,2009).

It has been suggested by Huhtanen andSveinbjörnsson(2006)thatenhancedstarchdigestionin the small intestine increases milk protein,perhapsbysparingaminoacidsfrombeingusedforgluconeogenesisintheliver.Theyreportastudyinwhichmilkproteinyieldwasslightlybutsignificantlyhigherformaizecomparedwithbarleysupplements.Contrarytothisconcept,increasingstarchdigestionintherumenisconsideredadvantageousintermsofmilkproteinyield,sinceitincreasestheenergysupplyformicrobialproteinsynthesisandthemetabolisable

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protein flow to the small intestine (Thair, 2012).Finally,Reynolds (2006) reports a study inwhichtherewasnoevidencethatthesiteofstarchdigestionincreasedmilkproductionorchangeditscomposition.

Final thoughts

Rumenfermentationofstarch-althoughitreducesenergy efficiency over the enzymatic digestion inthe intestine- determines its nutritional value forruminants.The rate and extent of ruminal starchdigestion alters pH, cellulolytic activity,microbialproteinsynthesis,methaneemissionsand,eventually,animalproduction.Thereisaconsiderablebodyofresearchondegradationpotentialofvariouscerealgrains, but little information on non-traditionalsourcesofstarchthatcouldreplacecerealgrainswhenavailabilityandcostsarecompetitive.Thestructuraltraitsofstarchfromthesesources,theirinteractionwithothercomponents,andtheeffectofprocessingshould be examined. In vitro digestion techniquesconstituteastartingpointforstudyingtheextentandkineticsofstarchdegradationfromnon-conventionalsources.

Starch is themain energy component used inruminants feed tomodulate ruminal fermentationandpromotesyncwith thenitrogensources.Moreresearchisrequiredtoevaluatetheeffectofusingoneormoresourcesof starch—withdifferentdegreesof degradability and processing—on protein useefficiency,milk yield and compositional quality.Studiesshouldfocusonadditionlevelsandnutrientcompositionof the foragebase accordingwith thestage of lactation and energy requirements of theanimal.

Acknowledgements

TheAdministrative Department of Science,TechnologyandInnovation(Colciencias,Colombia,call 569 of 2012. Code 1115+569-33874) andthe Sustainability Strategy 2014-2015 (CODI,UniversidaddeAntioquia,Colombia)supportedtheresearch project entitled “Evaluación in vitro e in vivodediversasestrategiasnutricionalesparamitigarlas emisiones demetanoy su impacto productivo,

reproductivo y económico en ganadería de lecheespecializadaenelnortedeAntioquia”,whichmadepossiblethisliteraturereview.

Conflict of interest

Theauthorsdeclaretheyhavenoconflictsofinterestwithregardtotheworkpresentedinthisreport.

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