milk fat globule membrane and buttermilks: from ... · milk fat globule membrane and buttermilks:...

BASE Biotechnol. Agron. Soc. Environ.201014(3),485-500 Focus on:

Milkfatglobulemembraneandbuttermilks:fromcompositiontovalorizationCarolineVanderghem(1),PascalBodson(1)(2),SabineDanthine(1),MichelPaquot(2),ClaudeDeroanne(1),ChristopheBlecker(1)(1)Univ.Liege-GemblouxAgro-BioTech.DepartmentofFoodTechnology.PassagedesDéportés,2.B-5030Gembloux(Belgium).E-mail:[email protected](2)Univ.Liege-GemblouxAgro-BioTech.DepartmentofIndustrialBiologicalChemistry.PassagedesDéportés,2.B-5030Gembloux(Belgium).

ReceivedonMarch12,2009;acceptedonSeptember11,2009.

Buttermilk,theby-productfrombuttermanufacture,islowcostandavailableinlargequantitiesbuthasbeenconsideredformanyyearsasinvaluable.However,overthelasttwodecadesithasgainedconsiderableattentionduetoitsspecificcompositioninproteinsandpolarlipidsfromthemilkfatglobulemembrane(MFGM).Theaimofthisreviewistotakestockofcurrentbuttermilkknowledge.Firstly,themilkfatglobulemembranecompositionandstructurearedescribed.Secondly,buttermilkanditsassociatedproductsaredefinedaccordingtothemilkfatmakingprocess.Structureandmeancompositionoftheseproductsaresummarizedfromrecentdairyresearchdataandrelatedtotechnologicalproperties,especiallytheemulsifyingpropertiesprovidedbyMFGMcomponents.Finally,newapplicationsarepresented, leadingtopromisingvalorizationsofbuttermilkanditsderivateproducts.Keywords. Milk fat globule membrane, buttermilk, butter serum, polar lipids, technofunctional properties, emulsifyingproperties.

La membrane du globule gras du lait et les babeurres : de leur composition à leur valorisation.Lebabeurreestunco-produitdel’industriebeurrièretroplongtempsnégligé,bienqu’ilsoitpeucouteuxetdisponibleengrandequantité.Depuiscesvingtdernièresannées,unregaind’intérêtluiesttoutefoisportéenraisondesacompositiontrèsspécifiqueenprotéinesetenlipidespolairesoriginairesdelamembraneduglobulegrasdulait(MFGM).L’objectifdecettesynthèsebibliographiqueestdefairelepointsurlesconnaissancesrécentesrelativesaubabeurre.Premièrement,lacompositionetlastructuredelaMFGMsontdécrites.Deuxièmement,desdéfinitionsdubabeurreetdesproduitsassociéssontprésentéesencequiconcernelemoded’obtentiondeceux-ci.Lastructureetlacompositionmoyennedecesproduitssontrésuméesetassociéesauxpropriétéstechnologiques, toutparticulièrementauxpropriétésémulsifiantesdescomposantsdelaMFGM.Finalement,denouvellesapplicationssontprésentéesafindepromouvoirlesvaleursajoutéesdubabeurreetdesesproduitsdérivés.Mots-clés.Membraneduglobulegrasdulait,babeurre,sérumdebeurre,lipidespolaires,propriétéstechnofonctionnelles,propriétésémulsifiantes.

1. IntroductIon

Buttermilkisthetermusedtorefertotheliquidphasereleased during churning (destabilization) of creamin the butter making process (Morin et al., 2007a).For many years, buttermilk has been considered asthe invaluable by-product of the milk fat industry.The worldwide production of buttermilk couldbe considered close to that of butter production(Morinetal.,2007a),whichwasestimatedataround8.6x 106tin2006(FAOSTAT,2006).FreshbuttermilkconsumptionremainsmarginalinEurope.Tocounter

the increasingsolidsdisposedaswaste,buttermilk isusedinanimalfeedordriedtobeincorporatedindairyorbakeryproductsasanemulsifyingagent.

Overthelasttwodecades,manystudiesreviewedin this paper have revealed new valorizationpotentialities for buttermilk, specifically as a sourceof high added-value components. Like skimmedmilkandwhey,buttermilkcontainslactose,minerals,caseins, and serum proteins which can be extracted,purifiedandvalorizedinverydistinctfoodornonfoodapplications. Additionally, buttermilk has attractedconsiderableinterestduetoitshighcontentofresidual

486 Biotechnol. Agron. Soc. Environ. 201014(3),485-500 VanderghemC.,BodsonP.,DanthineS.etal.

milkfatglobulemembrane(MFGM).Thisbiologicalmembrane ensures structural integrity, protectionand stability of the milk fat in the aqueous phase(Danthine et al., 2000; Ye et al., 2002). MFGMis released into the aqueous phase during creamchurning (destabilization of milk fat globules). Itcontains specific proteins and unique polar lipids(PL) closely associated into a complex structure.Some of these MFGM components are consideredbeneficial for theirvarioushealth-relatedproperties(Spitsberg,2005;Dewettincketal.,2008).Giventhisrich composition, buttermilk, whey buttermilk andotherby-productsderivedfromthemilkfatindustry,such as butter-serum, could open a wide range ofnewmeansofvalorizationasemulsifiers,stabilizers,andhealthpromotersinfoodornon-foodoutlets.

2. coMposItIon and structure oF the MILK Fat gLobuLe MeMbrane

Ithasbeenestimatedthatthemassofthemembraneoffatglobulesaccountsfor2-6%ofthetotalmassoffatglobules(Singh,2006).AsMFGMisabiologicalmembrane it is mainly composed of proteins,phospholipids,glycoproteins,neutrallipids,enzymesandotherminorcomponents(Danthineetal.,2000).The composition of the MFGM can vary widelydepending onmany factors such as fat content, fatglobulesize,diet,breed,healthandstageoflactationofthecows(Singh,2006).

2.1. Lipid composition of the milk fat globule membrane

Neutral lipidsaccount fora rangebetween56-80%of total lipids in theMFGM. Triglycerides are themajor fraction of neutral lipids (37-68% of totallipids).AmajorpartofthesetriglyceridesappeartooriginatefromcontaminationbythelipidcoreduringisolationoftheMFGM.Theotherneutrallipidsare:diglycerides (9%), monoglycerides (0.7%), esters(0.1-0.8%) and cholesterol (0.2-6.1%) (% of totallipids)(Danthineetal.,2000).

Polar lipids are composed of phospholipids andsphingolipids; they account for 15-43% of totallipidsintheMFGM(Danthineetal.,2000).Amongphospholipids, phosphatidylcholine (PC), andphosphatidylethanolamine (PE), are zwitterionicphospholipids thatarepresent in largequantities inthe MFGM isolate (35 and 30% respectively). Incontrast,anionicphospholipids,phosphatidylinositol(PI) and phosphatidylserine (PS) are present inloweramounts(5and3%respectively)(Dewettincket al., 2008). Three sphingolipids are also found:sphingomyeline (SM) (22%), lactosylceramide

(traces) and glucosylceramide (traces). Free fattyacidsandgangliosidesarealsofoundintheMFGMinminoramounts.

InarecentworkbyFauquantetal.(2007),usingagaschromatographycoupledwithamassspectrometryapproach, many minor bioactive sterols weredetected in theMFGM, e.g. lanosterol, lathosterol,desmosterol,stigmasterolandβ-sitosterol.

2.2. protein composition of the milk fat globule membrane

MFGMproteinsaccountonlyfor1-4%oftotalmilkprotein.Despitetheirlowlevelofabundance,MFGMproteins play an important role in various cellularprocesses and defensemechanisms in the newborn(Cavalettoetal.,2008).Dependingonthesource,theMFGMiscomposedof25-60%ofproteins(Danthineetal.,2000;Singh,2006).

Inthepast,identificationandcharacterizationofMFGMproteinsweremainly based on comparisonof electrophoretic mobilities, different staining ofthe gels, molecular cloning techniques, reactionwith specific antibodies, and identification byN-terminalaminoacidsequencing.Bythesemeans,majorbandswereseparatedandidentified:Mucin1,Xanthinedehydrogenase/oxidase,Mucin15,Clusterof Differentiation 36, butyrophilin, adipophilin,lactadherin, and fattyacidbindingprotein (Mather,2000). Later, proteomic approaches, includingmass spectrometric (MS) analysis, provided rapid,unambiguous information on protein identity andfurtheridentificationofminorproteins.Bymeansofaproteomicapproach,humanMFGMproteinshavebeen identified (Quaranta et al., 2001; Cavalettoet al., 2002; Charlwood et al., 2002; Fortunatoet al., 2003). More recently, four works werepublished concerning the identification of furtherbovine MFGM proteins by mass spectrometric(MS) analysis: one-dimensional gel electrophoresisfollowed by capillary liquid chromatography (LC)-nanospray- tandem mass spectrometry (MS/MS)using a quadrupole time-of-flight (Reinhardt et al.,2006), two-dimensional gel electrophoresis (2-DE)followed by reversed phase- LC-MS/MS (Fong etal., 2007), direct LC-MS/MS and 2-DE followedby matrix-assisted laser desorption/ionizationtime-of-flight MS (Smolenski et al., 2007), and2-DE followed bymatrix-assisted laser desorption/ionizationtandem-time-of-flight(Vanderghemetal.,2008). Despite great advancement in identificationofminorMFGMproteins,littleisknownabouttheirfunctionintheMFGM.

According to Keenan et al. (2006), about28differentenzymesorenzymaticactivitieshavebeendetected inMFGMpreparationsofcows’milk,e.g.

Valorizationofthemilkfatglobulemembrane 487

Xanthine dehydrogenase/oxidase, 5’-Nucleotidase,γ-Glutamyl transpeptidase, Catalase, Plasmin,Aldolase.Someoftheseenzymesmaypossiblycomefrommaterialentrainedincytoplasmiccrescents.

2.3. structure of the milk fat globule membrane

ThestructureoftheMFGM,inspiredfromthemodelsof Danthine et al. (2000), Evers (2004),Michalskietal.(2005)andKeenanetal.(2006),isschematicallyrepresentedinfigure 1.TheMFGMiscomposedofatri-layerstructure.First,thereisaninnermonolayerthat probably covers the intracellular lipid dropletsand that originates from the endoplasmic reticulumand possibly other intracellular compartments. Inthis monolayer, the hydrophobic tails of the polarlipidsare incontactwith the triglyceride-richcore.Secondly, an outer bilayer that originates from thesecretory cell apical plasma membrane, where theoutermost hydrophilic head groups of the polarlipidsareincontactwiththeaqueousphaseofmilk.Thisbilayerhas anelectron-densecoatmaterialonthe inner face. Some globules present inclusionscalled“cytoplasmiccrescent”entrainedbetweentheglobuleandthesurroundingmembrane(Danthineetal.,2000;Keenanetal.,2006).

Concerning the lipids, Deeth (1997) suggestedthatthepolarlipidsintheMFGMhaveanasymmetricdistribution like other biological membranes. TheoutsideofthemembraneismainlycomposedofPCandSM,andtheinnersurfaceismainlycomposedofPE,PSandPI.

Regarding the MFGM proteins, a number oftechniqueshavebeenemployedinthepast inorderto elucidate their disposition. These techniquescomprise: morphological studies by means ofelectron microscopy; surface studies such aslabeling techniques, use of lectins, enzyme attack,dissociating agents and detergents (McPherson etal., 1983). In these techniques, identification ofthe labeled surface proteins, peripheral proteinsreleased after utilization of dissociating agents, orproteins remaining after a proteolytic attack, wasbased principally on comparison of their relativeelectrophoreticmobilities inonedimension sodiumdodecylsulphate-polyacrylamidegelelectrophoresis.

Even ifmuchknowledgehasbeengainedaboutthedispositionoftheMFGMcomponents,questionsremainandthemodelneedstobedetailed.

3. deFInItIon, types and productIon oF butterMILK and butter seruM

Buttermilk is defined by the majority of authorsas the aqueous phase released during churning ofcream in the buttermanufacturing (Corredig et al.,1997;Sodinietal.,2006;Morinetal.,2007a).Thisglobal definition includes awide range ofmilk fatby-productswithvariouscompositionsaccordingtotherawmaterialused,pre-treatmentconditionsandbuttermakingprocess.

The production of dairy cream, butter andanhydrous milk fat (AMF) concentrates the lipid

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Figure 1. Milk fatglobulemembranestructure (inspired fromDanthineetal.,2000;Evers,2004;Michalskietal.,2005;Keenanetal.,2006;illustrationnottoscale)—Structure de la membrane du globule gras du lait (modèle inspiré de Danthine et al., 2000; Evers, 2004; Michalski et al., 2005; Keenan et al., 2006; le dessin n’est pas à l’échelle).


phaseofmilkandreleasestheserumaqueousphaseleading to skimmed milk, buttermilk and butterserum respectively. Each of these by-products hasitsspecificcomposition.Thecream,butter,AMFandby-products(buttermilk,wheybuttermilkandbutterserum) obtention process are presented infigure 2anddescribedinthissection.

3.1. cream obtention

Afterharvest,rawmilkiscoldstoredanddecreamedbycentrifugationtoadjustthefatcontentinskimmedmilk and concentratemilk fat globules into cream.This cream is generally normalized at around 40%fat and pasteurized.Thewhey produced by cheeseindustriesisweakenedincaseinbutcontainsresidualmilk fat globules. A whey cream is obtained bydecreamingofwheyanditcanbechurnedleadingtoawheybuttermilk.

3.2. butter process

The cream-to-butter transformation is a complexphenomenonduringwhichtheoil-in-wateremulsionis reversed into a water-in-oil emulsion leading toaqueousphaseseparation.

The complete explanation of the butter processhas been broadly detailed inMulder et al. (1974),Evers(2004)andFunahashietal.(2008).Thebutterprocess consists of 3 steps: ripening, churning andworkingwithwashing.

ripening. Ripening of pasteurized cream is afirst crucial step which influences both the fatglobule destabilization and sensorial quality ofbutter.Depending on ripening conditions includingtemperature, time and eventually added ferments,physical changes and biochemical reactions inducedifferent modifications. Physical treatment aims to

Figure 2. Outlineoftheobtentionprocessofcream,butterandanhydrousmilkfat—Schéma du procédé d’obtention de la crème, du beurre et de la matière grasse laitière anhydre.


managethemilkfatcrystallizationinordertoreducelipidlosesinbuttermilkduringchurningandtoshapethe butter texture. The biological ripening consistsof sowing pasteurized cream with specific lacticferments (starters, bacteria as Lactococcus lactissubsp.cremonis,Lactococcus lactis biovar.).Thesecultured cream starters lower acidity through lacticacidproductionanddeveloptypicalbutyricaromas.

Consequently,varioustypesofbuttermilkcanbeproducedfromripeningmilkfat.Inthemanufactureof European style butter, the churning of culturedcream produces cultured buttermilk. Commercialbuttermilk is sweet buttermilk, the by-product ofchurningsweetcreamintobutter(Sodinietal.,2006).

churning. Destabilization of milk fat globulesoccurs duringmechanical agitationof cream in thepresence of air, leading to disruption of the thinMFGM surrounding and stabilizing fat globules.Released fat aggregates into a solid lipid matrixformingbutter.DiscardedresidualMFGMfragmentsare recovered into the aqueous phasewithmost ofthe proteins, lactose andminerals contained in thecream(Corredigetal.,1997;Morinetal.,2006).

Following this same separation mechanismknown since Antiquity, the technological processof butter manufacturing has progressed fromdiscontinuous agitation in farm churns to differentcontinuous churning processes developed by thedairyfatindustry.Thephaseinversioninthebutter-making process iswidely dependent upon ripeningcreampropertiessuchascreamacidity, fatcontent,lipidcrystallization,MFGMstabilityandcontrolledtechnological parameters of temperature and shearrateonthebeater.TheeffectsofpH,fatglobulesize,fat content, churning time, and temperature profileandrotationratehavebeenstudiedbyMulderetal.(1974)intraditionalbuttermaking.

More recently, Funahashi et al. (2008)modeledtheinfluenceofchurningcharacteristicsincontinuousbutter manufacturing on the water content of thebutter.

Working and washing.Thechurningof40%milkfat cream presents an average butter yield of 50%,leadingtoaroughlyequalproductionofbuttermilkand butter (Morin et al., 2007a). The Food andAgriculture Organization of the United Nations(FAO)andWorldHealthOrganization(WHO)havenormalizedthewatercontentofbutteratamaximumof 16% (Funahashi et al., 2008). Consequently,the butter resulting from churning of fat globulesis washed with water, adjusted for salt, acidityand desirable aromas, before being mechanicallytexturedintoabuttermakingmachine,butyrificatorandchiller.

3.3. anhydrous milk fat process

The anhydrous milk fat (AMF) process is aninnovative way that the dairy lipid industry hasdeveloped to produce new fat productswith specifictechnofunctional properties. Based on the milk fatfractionation, the process leads to the separation ofAMFandbutter serum, the aqueous phase of butter.Afirstwayconsistsofmeltingstandardizedbutter(at50°C) and centrifuging it to enhance the separationofbutteroilandserum(processusedinthestudiesofRombautetal.,2006andBrittenetal.,2008).Asecondprocess described schematically in Pérennou (1999)concentratesstandardizedcreamfrom40%to70-80%before the phase inversion and the oil concentrationleadingtotheAMF.Thebuttermilkresultingfromthisprocess is decreamed; the lipid phase returns to thedestabilizationprocessandtheaqueousphaseiscalledbutterserumorbetaserum.

4. coMposItIon oF butterMILK and butter seruM

Many recent studies on buttermilk aim to assess thecompositional and functional properties of differentbuttermilks(Wongetal.,2003a;Govindasamy-Luceyet al., 2006; Sodini et al., 2006) and butter serum(Britten et al., 2008) or to evaluate the potentialitiestoconcentratecertainhigh-valuecomponentsfromthebuttermilk (Corredigetal.,1997;Morinetal.,2006;2007b;Rombautetal.,2007a;2007b).Thecompositionofdrymatter,lactose,proteins,totallipids,polarlipidsand ash in different types of buttermilk and butterserums presented in these works are synthesized intable 1andcomparedwiththecompositionofrawandskimmilk.

Buttermilkcontainslactose,mineralsandskimmedmilkproteins(caseinsandwheyproteins)inthesameproportion as skimmed milk (Corredig et al.,1997).However, the concentration of polar lipids on a drybasis inbuttermilkhasbeen reported tobe four,fiveandtentimeshigherthanthatinskimmedmilk,wholemilk and cream, respectively (Christie et al., 1987;Rombautetal.,2005).ThemajorityofpolarlipidsinmilkareoriginatedfromtheMFGMwhichisreleasedduring churning in the aqueous phase (Malin et al.,1994).AccordingtoMorinetal.(2007a),MFGMcouldrepresentlessthan5%oftotalsolidsinbuttermilk.

Exceptfortotallipidsandpolarlipids,theproteincontentofsweetandculturedbuttermilkiscomparablewith that of skimmed milk. Nevertheless, certainauthorsnoteaslightlylowerproteinconcentrationinsweetandculturedbuttermilkthanforskimmedmilk(25-36.5%comparedto36%)(Sureletal.,1995;Scottet al., 2003b; Sodini et al., 2006). Despite washing

490 Biotechnol. Agron. Soc. Environ. 201014(3),485-500 VanderghemC.,BodsonP.,DanthineS.etal.ta

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butter, a small quantity of proteins from sweet orcultured cream is lost in the butter.Wheybuttermilkpresents the lowest protein content (13.2-14.1%)dueto the coagulation of caseins during cheese making,during which a whey poorer in proteins is released(Sodinietal.,2006;Morinetal.,2006).

According toBritten et al. (2008), the proportionofproteinsinsweetbuttermilkisapproximately59%caseins, 23% serum proteins, mainly α-lactalbuminandβ-lactoglobulin,andaround19%MFGMproteins.Inaddition,caseinsareextractedinlargequantityfromwheybuttermilk,MFGMandserumproteinsconstitutethelargerpartofthisbuttermilk(Sodinietal.,2006).

Fat content in buttermilk is related to buttermanufacturing conditions and the effectiveness ofthe fat removal process during the post-treatment ofbuttermilk.This explains the variation of fat contentobservedamongsweet,culturedandwheybuttermilks(Elling et al., 1996; Sodini et al., 2006).Wee et al.(2003) studied the inconsistency of composition inbuttermilkpowder,whichcanleadtoinconsistencyoffinal product quality. They suggest that the differentcompositionofbuttermilkpowderinthemarketcouldbeduetothemanufacturingmethodandthesourceofmilk.Fatcontentvariesfrom4.6to14.5%indrymatterforsweetbuttermilkandcanreachnearly29%inwheybuttermilk.

In recent years, much attention has been paid tothepolarlipidsfromtheMGFM,whichhavebecomethemostwidelystudiedcomponents in recentpapersabout buttermilk. Polar lipid content in raw milkwaversbetween100and400mg.kg-1asafunctionofthefatcontent,season,stageof lactationandfeedingconditionsof the cows (Christie et al., 1987;Bitmanetal.,1990).Duringthebuttermakingprocess,thetotalpolarlipidsinitiallypresentinrawmilkaredistributedamong skimmed milk (52%), buttermilk (22%) andbutter (26%) according to Britten et al. (2008) inagreement with Christie et al. (1987) and Rombautet al. (2005). Phospholipids extracted from skimmedmilk during decreaming come from membranousmaterial and very small fat droplets initially presentin rawmilk (Anderson et al., 1975) aswell as fromMFGM fragments detached from fat globules duringthe centrifugal process (Walstra et al., 1982). It isbelieved that the migration of lipids from MFGMto the serum only occurs in the presence of serumcomponents (Houlihan et al., 1992). The polar lipidcontentindifferenttypesofbuttermilkrangesfrom1.2to2.1%indrymatter.Pérennou(1999),confirmedbyrecentresultsofBrittenetal.(2008),showedthatbutterserum contains a higher proportion of phospholipids(up to 1 g.100 g-1 of fresh product). Rombaut et al.(2005)obtainedaphospholipidcontentof11.5%(w/w)in drymatter in a butter serum and recommend thisby-productasaninterestingsourceofpolarlipids.

No significant difference was observed betweenskimmedmilkandsweetbuttermilkinrelationwiththeproportionofpolarlipids.Nevertheless,Rombautetal.(2005)andBrittenet al. (2008)notedanenrichmentof sphingomyeline in butter serumat the expense ofphosphatidylethanolamine. The composition of polarlipids obtained in sweet buttermilk is PE39.0%,PC24.4%,SM19.3%,PS8.3%,andPI8.9%,whereas,forbutterserumthepolarlipidsdistributionisPE29.2%,PC 24.9%, SM 26.8%, PS 10.1%, PI 9.1% and PS8.3%(Brittenetal.,2008).

5. butterMILKs and MILK Fat gLobuLe MeMbrane FractIons: FunctIonaL propertIes

TheprincipalfunctionofMFGMinmilkistostabilizethelipiddropletsintheplasma.Thisfunctionisvaluedbytheutilizationofbuttermilkasanaturalingredientinfoodprocess.TheaimofthissectionistoreviewthestudiesconcerningthefunctionalpropertiesofMFGMfractionsandbuttermilk.

5.1. emulsifying properties of milk fat globule membrane fractions and buttermilk

Anykindofbuttermilk,wheybuttermilkorbutterserumis found to contain two main types of emulsifyingagents: proteins like caseins, whey proteins andMFGM proteins; and lipids like polar lipids derivedfromtheMFGM.

The surface active properties of milk proteins,which have been largely described in the works ofShimizu et al. (1983), Dickinson (1989), Dickinsonet al. (1989), Horne et al. (1995), and Britten et al.(1991),arebrieflypresentedhere.

Caseinsarethemajorproteinsofbovinemilkandhave been extensively studied separately from othermilkconstituents.Theseareknowntohaveadisorderedstructure due to their high proline content (Brittenetal.,1991).Inaddition,theyareflexibleproteinsandhaveamphiphilicpropertiesintheirprimarystructuresthatallowadsorptionattheinterfaces(Shimizuetal.,1983).Inparticular,ß-casein,attheinstantoffoamingoremulsification, isable to reduce tension rapidlyatthenewlyformedinterface(Dickinsonetal.,1989).

Concerning whey proteins, these are globularstructured proteins. They do not lower the surfacetension as quickly as caseins but are able to form atightly-packedviscoelastic structureat the interfaces,favoringlong-termstability(Dickinsonetal.,1989).

WithregardtotheemulsifyingcomponentsoftheMFGM:membraneproteinsandphospholipidscouldbe considered as natural emulsifying agents due totheiramphiphilicnature.


In the following section the fundamental studiesconcerningtheemulsificationpropertiesoftheMFGMaresummarized.

Fundamental studies on the native milk fat globule membrane. The first role of fat globule membraneis to stabilize the fat in milk. According to Phippset al. (1982), the interfacial tension of fat globulesis inferior to2mN.m-1andthatcouldexplaininpartits emulsifying properties. Some studies have beenfocusedon theemulsifyingand surfacepropertiesofrawandpuremilkfatglobulemembranecomponentsandarepresentedbelow.

Among the first studies, Shimizu et al. (1980)studiedtheroleofMFGMproteinsandphospholipidsin the stabilization of fat globules in milk. WhenproteinsoftheMFGM,obtainedfromawashedcream,weredigestedbypapain, thedecreasein thestabilityofthecreamwasconsiderableduetoclusteringofthefat globules. These results suggest that proteins andglycoproteins inMFGMmay play an important roleinthestabilizationoffatbyinterruptingclusteringoffatglobules.Inaddition,removalofthephospholipid’spolar head group by phospholipase C produced amarkeddecreaseinthestabilityofthecreamemulsionrelatedtoacoalescenceoffatglobulesandoiling-off.Shimizu et al. (1980) concluded that phospholipidsinterruptcoalescenceof fatglobulesby therepulsiveforces derived from the ionogenic groups of thephospholipids.

Subsequently, Kanno (1989) demonstrated thatMFGM suspension extracted from fresh raw milkcouldsuccessfullyemulsifybutteroilandyieldstableemulsions.Differentconcentrationsofmembraneweretested in order to assess the emulsion stability, thewhippabilityandthefoamstability.Theyfoundthatat2%MFGM(80mgofMFGM.g-1offat),emulsifyingactivityandemulsionstabilityweremaximal.

Usingthefilmbalancetechnique,Innocenteetal.(1997) studied thesurfaceandmechanicalpropertiesof a soluble fraction of MFGM obtained from rawcream.The experimentswere performed at differenttemperatures in order to imitate the conditions ofdifferent dairy-food processing operations such asheat treatments,milkcreamripeningandmechanicaltreatments.ThisstudyclearlyshowsthattemperaturegreatlymodifiesthesurfacepropertiesofMFGMfilms.These changes were associated with the percentageof crystalline triglycerides and the phospholipidstransition(Innocenteetal.,1997;Danthineetal.,2000;LaadharKarrayetal.,2006).

Finally, Corredig et al. (1998c) characterized theinterface of emulsions prepared with a fraction ofMFGM isolated from fresh raw cream. Proteins andphospholipids fromtheMFGMwereadsorbedat theinterface forminganewmembrane thatwasaffected

very little by the presence of surfactants such asTweensandTriton-Xandproteinssuchascaseinsandβ-lactoglobulinadded to theemulsion.Thisbehavioris very different from that of emulsions stabilizedby other milk proteins. They concluded that thephospholipidspresentintheMFGMmaterialadsorbedattheinterfaceloweredtheinterfacialtension,causingagreaterresistancetofurtherexchangeofsurfactant.

emulsifying properties of industrial buttermilk and isolates.TheutilizationofpureMFGM,extractedfromrawcream, as a functional ingredient is not possiblefromaneconomicpointofview(Danthineetal.,2000).However,theMFGMpropertiescouldbevaluedintheby-productofbuttermanufacture,buttermilk.Thereisan increasing interest in isolating theMFGM and/orspecificfractionsfromdairyproductsandby-products(Dalemansetal.,2008).Theemulsifyingpropertiesofbuttermilksandisolatesarediscussedinthefollowingsection.

According toElling et al. (1996) andScott et al.(2003a)MFGMfragmentsreassociatetotheinterfaciallayer during the recombination of creamwith sweetbuttermilkandbutterderivedaqueousphase.Similarfindings were reported by Corredig et al. (1998a).Theypreparedemulsionswithcommercialbuttermilkand soybean oil and analyzed the surface coverageof protein adsorbed at the interface by SDS-PAGE.They found that caseins,MFGM proteins and wheyproteins were present. Caseins made up about 50%of the total protein adsorbed. Elling et al. (1996)stated that the amount of phospholipids incorporatedin the reconstituted membrane could vary if thehomogenizationpressureiscontrolled.

Functional properties of commercial buttermilksolids have been compared to skimmed milk andwhey in oil-in-water emulsions.Wong et al. (2003a)reported that commercial buttermilk showed limitedfunctional properties beyond emulsification capacityand stability over those observed for skimmedmilk.In contrast, Scott et al. (2003a) demonstrated thatbuttermilkemulsionsremainedstableforalongertimeduring storage compared to creams formulated withskimmed milk. Their findings were corroborated byotherinvestigators(Sodinietal.,2006)whofoundthatdifferentkindsofbuttermilk(commercialsweet,sourand whey buttermilk) showed higher emulsificationpropertiescomparedtoskimmedmilkandwhey.

Several studies have focused on obtainingconcentrated MFGM isolates from an industrialsource of buttermilk. Corredig et al. (1997) isolatedmembrane-derivedmaterialfromanindustrialsourceofbuttermilktoinvestigatethepotentialutilizationoftheby-productinoil-in-wateremulsions.TheMFGMisolates were obtained from commercial buttermilkby ultracentrifugation following the addition of


sodiumcitrate todissociate the caseinmicelles.ThisMFGMisolateprovedtohaveverypooremulsifyingproperties compared to thewhole buttermilk isolate.The authors concluded that heat treatment of creamat source and churning causes a high degree ofaggregation and changes in the functional propertiesof membrane proteins and phospholipids. A similarworkwasundertakenbyRoeschetal.(2004)whenthedifferences in functionality betweenMFGM isolatesandabuttermilkconcentrateweretested.Theirstudiesdemonstrated that MFGM isolates, obtained fromrepresentativehighlyheat-treatedbuttermilk, showedbetter creaming stability and smaller oil droplet sizedistributionthanwholebuttermilkconcentratesamples.ThesefindingsweredifferentfromthepreviousresultsonMFGMisolates. It shouldbeemphasized that thevariability and quality of cream, pre-treatment ofcreamduringprocessingofbutterand themethod toobtain concentrated MFGM isolates could influencethe final functionality. The same group (Corredigetal.,1998b)investigatedthechangesoccurringintheMFGMwhencreamwasheatedbeforebutter-making.Heat treatmentof thecreamcausedwheyproteins toassociatewiththeMFGM,affectingthesolubilityanddiminishing the amount of iron and the emulsifyingpropertiesoftheMFGMisolates.Eventemperaturesaslowas65°Cstronglyaffectedthefunctionalpropertiesofthemembranefraction.RecentworkconductedbyGassi et al. (2008) shows that the heat treatment ofcreamaffectsthephysicochemicalpropertiesofsweetbuttermilk. The heat treatment induced a significantdecrease in soluble protein content in buttermilks aswellasanincreaseinthebuttermilkphospholipid/fatratio.

Studies on the functionality of buttermilk arepromising.However,more research isneeded in thisfield.Theemulsifyingpropertiesofbutterserumcanbe determined and compared to that of buttermilk.Moreover,noworkhasbeenfocusedonthestabilityofreconstitutedbuttermilkemulsionandtheresistanceofthemembranetowardscoalescence.Nevertheless,themost typical defect related to recombined emulsionsis the phase separation and coalescence of dropletsduring quiescent storage (Dalgleish, 2004). Optimalformulation and high qualitymembranematerial arefundamentalforthepreventionofcoalescenceforlongshelf-lifeproducts.

5.2. applications of buttermilk and milk fat globule fractions in food: physico-chemical, technofunctional and sensory properties

The economic and ecological valorization of aby-product such as buttermilk is obvious. To ourknowledge, at present the industrial applications ofbuttermilkarelimitedtotheadditionofthisby-product

inrecombinedcreamandbread.However,thescientificliterature pointed out new properties and suggestedthe utilizations of buttermilk andMFGM isolates ina rangeof other foodstuffs. In this section, scientificworks regarding the applications and properties ofMFGMfractionsandbuttermilkinfoodaredescribed.

The applications are mainly oriented to thedairy sector in products such as recombined cream,recombinedevaporatedmilk,yogurt,cheddarcheese,mozzarella, pizza cheese and low fat cheese. Othernon-dairy product applications are bread and naturaljuice. The modified properties in the final productsinclude emulsification, stability, moisture retention,yield,heatstability,textureandflavor(table 2).

Singhetal.(1990)’sfirststudiesinthedairysectorevaluated the effect on heat stability of recombinedevaporated milk by adding 10% (v/v) of freshbuttermilktoskimmedmilk.Theauthorsshowedthatoverallstabilitywasincreasedinmilkcollectedduringthe period fromOctober toMarch, but the extent ofstabilization varied. The composition of the newlyformed fat globule membranes is a major factor indetermining heat stability. The authors hypothesizedthatsurface-activeagentsinbuttermilk(phospholipidsandlipo-proteins)displacedskimmedmilkproteinfromthe membrane during homogenization. The authorsstatedthatfurtherresearchisneededontheeffectsofhomogenization and the adsorption of proteins ontofatglobulesinrelationtoheatstabilityofrecombinedevaporatedmilk.

In dairy emulsions, based on their emulsifyingproperties, the use of buttermilk andMFGM isolatein recombined oil-in-water emulsions considerablyreducedtheparticlesize(Roeschetal.,2004;Sodiniet al., 2006) and enhanced creaming stability (Scottetal.,2003a;Roeschetal.,2004).

Concerning cheeses, in an earlier study, Law etal. (1973) investigated the influence of the MFGMaddition (by varying the concentration of buttermilkaddition) on flavor and lipolysis of cheddar cheese.Theirstudyhaddemonstratedthattheflavorofcheddarcheeseisnotextensivelyaffectedbytheconcentrationof phospholipids in the formulation.They concludedthat development of the typical flavor of cheddarcheeseismainlyduetotriglycerides.However,MFGMmaterialcouldpreventanundesiredrancidflavor,asitadsorbsattheinterface,protectingthelipidcorefromexcessivelipolysis.Incontrast,inthereviewofJoshietal.(1994),duringtheripeningstage,theproteolysisand the lipolysis increased in the different types ofcheese containing buttermilk solids compared to thecontrol sample.Thesefindingswere corroboratedbytheresearchofMayesetal.(1994).Intheirstudytheyfoundthattheadditionofrawbuttermilkhomogenizedwithcreamfor themanufacturingof low-fatcheddarcheese slightly improved the textural and flavor


table 2. Effectoftheadditionofbuttermilkandmilkfatglobulemembrane(MFGM)isolatesinfoodonthephysico-chemical,technofunctionalandsensoryproperties—Effet de l’addition du babeurre et d’isolats de la membrane du globule gras du lait (MFGM) sur des propriétés physico-chimiques, technofonctionnelles et sensorielles d’aliments.

product application physico-chemical, effect Form of buttermilk references technofunctional, sensory propertiesRecombinedevaporated Heatstability Stabilityincreased Freshbuttermilk Singhetal,1990milkRecombinedcream Stability Enhancementin Sweetbuttermilk Scottetal.,2003a creamingstability Butter-derivedaqueous phase Featheringstability Moreresistant Sweetbuttermilk Scottetal.,2003a towardsfeathering Butter-derivedaqueous phase Viscosity Increasedfluidity Sweetbuttermilk Scottetal.,2003a Butter-derivedaqueous phase Flavor Creamyflavor Sweetbuttermilk Scottetal.,2003a Butter-derivedaqueous phaseOil-in-wateremulsions Emulsification Reductionofparticle Sweetbuttermilkpowder Sodinietal.,2006 sizeinemulsion Sourbuttermilkpowder Commercialsweet Buttermilkpowder MFGMisolateobtained Roeschetal.,2004 frombuttermilkby additionofsodium Goodstabilityto MFGMisolateobtained Roeschetal.,2004 creaming frombuttermilkby additionofsodium citrateandmicrofiltrationLowpHoil-in-water Emulsification Reductionofparticle Wheybuttermilkpowder Sodinietal.,2006emulsions sizeinemulsionCheddarcheesewith Emulsification Reductionoffreeoil Ultrafilteredsweet Mistryetal.,1996reducedfat buttermilk Ravaletal.,1999 Moistureretention Increasedwater Ultrafilteredsweet Mistryetal.,1996 retentionofcurd buttermilk Highermoisture Sweetbuttermilkand Turcotetal.,2001 content ultrafilteredbuttermilk retentate Highermoistureinfat- Rawsweetcream Mayesetal.,1994 freesubstance buttermilk Yield HigherCheeseyield Ultrafilteredsweet Mistryetal.,1996 buttermilk Sweetbuttermilkand Turcotetal.,2001 ultrafilteredbuttermilk retentate Texture Decreasedhardness, Ultrafilteredsweet Mistryetal.,1996 increasedbodyand buttermilk texture Decreasedhardness, Sweetbuttermilkand Turcotetal.,2002 elasticityandcohesion ultrafilteredbuttermilk Increasedadherence retentate Softerandsmoother Rawsweetcream Mayesetal.,1994 buttermilk Meltability Reducedmeltability Ultrafilteredsweet Ravaletal.,1999 buttermilk Flavor Flavorimprovement Rawsweetcream Mayesetal.,1994 buttermilk


characteristics of cheese. They hypothesized thatbuttermilk enzymes could act on the lipid substrate.MoreevidenceispresentedbySamples(1985),wherehe found that active n-glutamyl transpeptidase wasrelated to twomajor volatile compounds in cheddarcheese.HepointedoutthatMFGMisasourceofthisenzyme.

Later, the inclusion of 5% of concentrated ultrafiltered sweet buttermilk in different types of low-fat cheddar or mozzarella cheese, reduced free-oilformation (Mistry et al., 1996; Poduval et al., 1999;Ravalet al.,1999).Theemulsificationof fat in such

cheesetypescouldbeimprovedbythephospholipidscontainedinbuttermilk(Ravaletal.,1999).

Another interesting property observed in cheesesenrichedwithbuttermilkwasanincreasedcheeseyield(Mistryetal.,1996;Turcotetal.,2001;Govindasamy-Luceyetal.,2006)duetothewaterretentioncapacityofphospholipidsanddenaturedwheyproteins(Turcotet al., 2001). However, high water retention couldimpartnegativeeffects incheese suchan increase inthe acidity during the ripening period (Joshi et al.,1994),reductionoftheshelflifeandmodificationsinthetexture.

table 2. Effectoftheadditionofbuttermilkandmilkfatglobulemembrane(MFGM)isolatesinfoodonthephysico-chemical,technofunctionalandsensoryproperties—Effet de l’addition du babeurre et d’isolats de la membrane du globule gras du lait (MFGM) sur des propriétés physico-chimiques, technofonctionnelles et sensorielles d’aliments(continued).

product application physico-chemical, effect Form of buttermilk references technofunctional, sensory propertiesCheddarcheese Viscosity Higherapparent Ultrafilteredsweet Ravaletal.,1999 viscosity buttermilk

Flavor Preventrancidflavor Sweetcreambuttermilk Lawetal.,1973Mozzarellacheesewith Emulsification Reductionoffreeoil Ultrafilteredsweet Poduvaletal.,1999reducedfat buttermilk Moistureretention Highermoisturecontent Ultrafilteredsweet Poduvaletal.,1999 buttermilk Texture Decreasedhardness, Ultrafilteredsweet Poduvaletal.,1999 increasedbodyand buttermilk texture Meltability Reducedmeltability Ultrafilteredsweet Poduvaletal.,1999 buttermilk Pizzacheese Moistureretention Highermoisturecontent Condensedsweet Govindasamy- creambuttermilk Luceyetal,2006 Yield Highercheeseyield Condensedsweet Govindasamy- creambuttermilk Luceyetal,2006 Texture Decreasedchewy Condensedsweet Govindasamy- creambuttermilk Luceyetal,2006 Meltability Reducedmeltability Condensedsweet Govindasamy- creambuttermilk Luceyetal,2006 Coagulation Weakeningoftherennet Condensedsweet Govindasamy- properties gel creambuttermilk Luceyetal,2006Nonfat/lowfatyogurt Texture Softerandsmoother Ultrafilteredsweet Trachooetal.,1998 buttermilk Commercialsweet buttermilkpowder Viscosity Increasedviscosity Ultrafilteredsweet Trachooetal.,1998 buttermilk Commercialsweet buttermilkpowderBread Moistureretention Higherwaterabsorption Buttermilk Bilginetal.,2006 ofdough Dough’sproperties Increasedresistanceto Buttermilk Bilginetal.,2006 extensionandenergy values Sensoryproperties Bettersensoryscore Buttermilk Bilginetal.,2006


Arecentstudy,conductedbyMorinetal.(2008),showsthatheattreatmentofthecreamisanimportantreason for the buttermilk coagulation problems incheeses.

Pasteurization of creammodifies the surface ofMFGMparticles,andthismayexplainwhybuttermilkhaspoorcoagulationpropertiesandthereforeyieldsrennetgelswithtexturedefects.

Ultrafiltered buttermilk could be used as asuitable ingredient to manipulate the degree ofmelting (Poduval et al., 1999). In reduced-fatcheddarcheese,mozzarellacheeseandpizzacheese,additionofbuttermilk reducedmeltability (Poduvaletal.,1999;Ravaletal.,1999;Govindasamy-Luceyetal.,2006).Poduvaletal. (1999)andRavaletal.(1999) hypothesized that the components of theMFGMformedanintegralpartoftheproteinmatrixandcausedmoreextensivecrosslinks,resultinginastructurethatdidnotmeltwell.

Furthermore,theadditionofbuttermilkdecreasedhardness, increased body and improved the textureofcheeses (Mayesetal.,1994;Mistryetal.,1996;Poduvaletal.,1999;Turcotetal.,2002).Similarly,theadditionofupto4.8%sweetbuttermilkpowderto low fat yogurt enhanced its sensory qualitiesby softening the product and making it smoother(Trachooetal.,1998).

Recentlyevidencewaspresentedthatbuttermilksolids cause antioxidant activity by acting as areducing agent to scavenge peroxide and hydroxylradicalandsequesterbothFe+2andFe+3(Wongetal.,2003b). The authors recommend the utilizationof buttermilk in foods in order to prevent lipidperoxidation.

Buttermilk is also used in baked goods becauseofitstypicalflavor(Malinetal.,1994;Bilginetal.,2006) and also has a retarding effect on crumbfirmness(Bilginetal.,2006).

Anotherinnovativeutilizationofbuttermilkisthesupplementationofnaturalfruitbeverageswiththisby-product(Farahetal.,1981;Shuklaetal.,2004).Thesefruitbeveragescombinethehighproteinandmineralcontentsofbuttermilkwith thevitaminsofthefruitinacheaperproduct.

In conclusion, different types of buttermilk andMFGMisolateshavebeenproventobesuccessfulinimprovingsomefoodcharacteristics.Anexampleistheeffectofbuttermilksupplementationonreducedfat cheeses, as it givesproducts characteristics thatare similar to or better than those of their full fatcounterparts.However, the quantities of buttermilkusedasafoodingredientmustbecarefullymeasuredso as to avoid affecting the functional and sensoryproperties of final products. High concentrationscouldnegativelyaffecttheirpropertiesandresultinthedevelopmentofoff-flavors.

5.3. other applications of the milk fat globule membrane: pharmaceutical applications and formation of liposomes

Conventional phospholipids could be obtainedfrom natural origins such as soybean, egg yolk orsynthesized by various fatty acid compositions.Asfor the other sources, the phospholipid fractionsfrom the MFGM could be used for emulsionsor liposome formulations for pharmaceutical orcosmeticapplications.Moreover, thespecial,uniquecomposition of the MFGM phospholipids fraction(50%saturated,35%monounsaturatedand15%poly-unsaturated fatty acids) makes products resistant tooxidation.

Due to their natural origin, MFGM componentsmaybesafefororaladministration,and theyareaninterestingalternativetosyntheticemulsifiers.MFGMhas been tested as a novel emulsifier to enhanceintestinal drug absorptionofvitaminD3 (Liu et al.,1991),epidermalgrowthfactor(Adachietal.,1993),α-linolenicacid(Yuasaetal.,1994)andcyclosporine(Satoetal.,1994).

TheMFGMcontainsatypeofsphingolipidfoundin animal cellmembranes: the SM.As presented inpoint 2.1., among sphingolipids, SM is present inlarge quantities.Malmsten et al. (1994) studied theproperties of SM extracted from bovinemilk.TheyfoundthatthephysicochemicalpropertiesofSMfrombovinemilkaresimilartothoseofsaturedPC.Theydemonstrated that itwaspossible toformliposomesreadily in the presence of cholesterol. SM frombovinemilkcouldbeusedforliposomedispersionsinordertobeusedasdrugdeliverysystemsandinthepreparationofemulsionsfordermalapplicationsandcosmetics.

Later,Miura et al. (2004) tested the emulsifyingpropertiesofbovinemilkphospholipidsbyreconsti-tuting cream using butter oil. They found thatphospholipids extracted frombovinemilk dispersedin the oil phase stabilize the oil-in-water emulsion.Additionally, the major polar lipids from bovinemilk (PC, PE and SM) were studied separately fortheir emulsifying properties. They reported thatPC dispersed in butter oil was able to prevent thesolidification of the emulsion, whereas PE and SMhad no such effects. The author hypothesized thatthe structural differences of the phospholipids maygiverisetothedifferentabilitiesofphospholipidstostabilizeemulsions.

Recently, Thompson et al. (2006b) producedliposomesfromaphospholipid-richMFGMfraction,using a microfluidizer.With this technique, a largevolumeofliposomescanbeproducedinacontinuousand reproducible manner, avoiding the use ofdetergents, solvents or alcohol. Milk fat globule


membraneliposomesaremorestablethantheirsoyacounterpartsinarangeofpHconditions,atavarietyof storage and processing temperatures, and in thepresence ofmono- and divalent cations (Thompsonetal.,2006a).

6. concLusIon

This literature review revised the recent advancesin composition and structure of the MFGM, butterserumsandbuttermilks,anddescribedthefunctionalpropertiesoftheseproducts.

Bymeansofnewmethods,greatadvancementinidentificationofminorcomponentsoftheMFGMhasbeen reached. However, little is known about theirfunctionintheMFGMstructureandtheirbiologicalfunction.Inparallel,muchknowledgehasbeengainedabout thedispositionof theMFGMcomponentsbutthestructureisnotknownindetailandworksdoneonthesubjectarenotalwayscoincident.

Although buttermilk has been considered asan invaluable by-product of the milk fat industry,recently it has attracted considerable interest due toitshighMFGMcontent.

Studies on the functionality ofMFGM fractionsand buttermilk are promising; they have beenproven to be successful in improving some foodcharacteristics.However,moreresearchisneededinthisfield(e.g.studiesontheinterfacialpropertiesofMFGMandbuttermilk;assessmentofthestabilityofreconstitutedbuttermilk emulsionand the resistanceofthemembranetowardscoalescence;effectofheattreatment of cream at source in MFGM fractionsor buttermilk, in the functional properties of finalproducts).Inaddition,otherby-productsderivedfromthemilkfatindustry,suchasbutterserum,remaintobeexploredfortheirfunctionalproperties.

MFGMfractionsandbuttermilkoffermanyotherpossibilitiesthatcanbeexploitedbyfoodtechnologists.The polar lipid fraction of the MFGM, in additionto having good emulsification properties in foodformulation,couldbeusedsafelyforpharmaceuticalpreparationof emulsions fororaluse and liposomalformulations.Anotherwayoffurtherenhancingtheseby-productsistoobtainmorespecificfractionsandtofindwiderapplicabilityandhigh-valueapplications.

Inconclusion,theMFGMtopichasbeenstudiedfor long timeandcontinues to interest thescientistsand technologists.Theknowledgeabout theMFGMandbuttermilkhasincreasedinthelastyearsduetotheuseofmoresophisticatedanalyticaltechniques.Inparallel, the studieson isolation/crackingofMFGMfromindustrialsourcesandthenumberofapplicationsof the MFGM and its fractions have considerablyincreasedasdenotedbytheresearchliterature.

List of abbreviations

2-DE:two-dimensionalgelelectrophoresisAMF:anhydrousmilkfatLC:liquidchromatographyMALDI-TOF:matrix-assistedlaserdesorption/ionization time-of-flightMFGM:milkfatglobulemembraneMS:massspectrometryMS/MS:tandemmassspectrometryPC:phosphatidylcholinePE:phosphatidylethanolaminePI:phosphatidylinositolPL:polarlipidsPS:phosphatidylserineSM:sphingomyelin

acknowledgement

ThefirstauthorgratefullythankstheUniversityofLiege-GemblouxAgro-BioTechforagrant.

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