Biochemical Characteristics of Ewe and Goat Milk (2011)

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Small Ruminant Research 101 (2011) 3340

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Small Ruminant Research

j ourna l homepage: www.e lsev ier .com/locate /smal l rumres

Biochemical characteristics ofewe and goat milk: Effect on the qualityofdairy products

Marzia Albenzio , Antonella Santillo

Department of Production and Innovation inMediterraneanAgriculture and Food Systems, University of Foggia, ViaNapoli, 25, 71100, Foggia, Italy

a r t i c l e i n f o

Article history:

Available online 2 October 2011

Keywords:

Milk technological properties

Cheese quality

Texture

Flavour

Biofuncional molecules

a b s t r a c t

The objective ofthis review paper is to report research findings on the role ofmilk protein

and indigenous enzymes on the ability ofewe and goat milk to be processed and on the

quality ofdairy products. Emphasis is placed on the role ofcasein characteristics and of

indigenous enzymes on flavour, rheology, texture, and biofuncionality of ewe and goat

cheese.

Finally, the review highlights that further study is needed on milk protein genetic vari-

ants in ovine species, and on the role ofindigenous enzymes, especiallyminor proteolytic

enzyme systems, on the quality ofsmall ruminantsmilk and dairy products.

2011 Elsevier B.V. All rights reserved.

1. Introduction

Milk protein and indigenous enzymes impact directly

on the ability ofmilk to be processed and on the quality of

dairyproducts.Thecharacteristics ofcaseinin eweandgoat

milk are of particular interest due to the high number of

polymorphism thatare related to cheesemakingproperties

of milk. Indigenous enzymes in small ruminant milk have

receivedminor attention than bovinemilk and focused on

the principal enzyme complex as plasmin and lipoprotein

lipase. Ewe and goat milk is mainly processed to cheese,

which are in increasing demand, therefore there is a need

of knowledge on the role of indigenous proteoliytic and

lipolyticenzymes on thecheesemakingability andon their

effects onripeningprocess.Biofuncionalityin eweandgoatmilk and dairy products is a new and much unexplored

research field which could be of particular significance for

the exploitation of small ruminant production.

The purpose of the present review is to report the role

of casein characteristics and indigenous enzymes on (i)

This paper is part of the special issue entitled Products from Small

Ruminants, Guest Editedby A. Govaris andG.Moatsou. Corresponding author. Tel.: +390881 589327; fax: +390881 589301.

E-mail address:[email protected] (M. Albenzio).

cheesemaking properties of ewe and goat milk; (ii) the

quality of cheesewitha particular reference toflavour, rhe-ology, and texture.Moreover, recent research are reported

on biofunctional compounds in ewe and goat milk and

dairy products.

2. Influence of casein polymorphismon

cheesemakingproperties of ewe and goatmilk

The genetic polymorphisms of milk proteins are of

importance as they areassociated toquantitativeandqual-

itative parameters in milk. Protein composition affects

technological properties of milk especially in cattle and

goatswhile in sheep theresults arecontroversial (Giambra

et al., 2010). Genetic polymorphisms of milk proteins alsoplay an importantrole inelicitingdifferent degreesofaller-

gic reaction (El-Agamy, 2007; Park, 1994; Saini and Gill,

1991). Some studies revealed that goat milk (Bevilacqua

et al., 2001; Slacanac et al., 2010) can be considered as a

proper alternative to human milk due to hypoallergenic

properties of its proteins.

Extensive investigation in goat milk revealed the pres-

ence of high numbers of alleles at the four casein loci

(Albenzio et al., 2009a; Kpper et al., 2010; Moioli et al.,

2007; Sacchi et al., 2005; Roncada et al., 2002): the

casein polymorphism is associated with different casein

0921-4488/$ see frontmatter 2011 Elsevier B.V. All rights reserved.doi:10.1016/j.smallrumres.2011.09.023
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34 M. Albenzio, A. Santillo / Small Ruminant Research 101 (2011) 3340

synthesis levels and different rate of phosphorylation of

the peptide chain (Albenzio et al., 2009a; Grosclaude et al.,

1994; Martin, 1993; Park et al., 2007). Goat milk from

animals with strong alleles have been associated with

higher cheeses yields and firmer curds thanmilk fromani-

mals with weak alleles (Albenzio et al., 2009a; Clark and

Sherbon, 2000; Tziboula-Clarke, 2003). Also -CN poly-morphisms i.e. levelsof glycosylationandphosphorylation

affects the susceptibility of goat milk to clotting enzymes

(Amigo et al., 2000) with important technological impli-

cation by influencing the coagulation stages of renneting.

Albenzio et al. (2009a) set a multiple covariance analy-

sis including casein genotype, SCC, goat milk composition

as factors able to account for milk coagulation properties.

Results evidenced that caseingenotypewas the factor that

accounted for a significant percentage of the total vari-

ability for goat milk renneting parameters (i.e. r, k20 and

a30). The study of goat casein loci permits to differentiate

goat population on the basis of milk utilization: animals

with weak or null casein alleles should be used in breed-

ingprograms aimedatproducingmilkwith hypoallergenic

properties andanimalswith strongalleles to improvequal-

ity and properties of milk and related products (Albenzio

et al., 2009a; Roncada et al., 2002; Sacchi et al., 2005).

The knowledge ofmilk protein genetic variants ismore

fragmentary in ovine species and is still limited to s1-CN and -LG loci, giving less conclusive results than ingoats (Amigo et al., 2000; Barillet et al., 2005; Moioli et al.,

2007). For their low frequency, the effects of casein poly-

morphisms on dairy traits or technological properties of

ewe milk are too inconsistent for implementing selection

(Barillet et al., 2005). The study of ewe casein variants

represent an effective approach to identify association to

economic traits to improve sheep breeds for specific milk

protein production (Barillet, 2007; Giambra et al., 2010).

3. Role of indigenous enzymes on cheesemaking

properties of ewe and goatmilk

Recent reviewreportedfindingsaboutindigenousenzy-

matic activity in ovine and caprine milks in relation to

equivalent bovine milk enzyme (Moatsou, 2010). Indige-

nous enzymes ineweandgoatmilk aremainlyrepresented

by plasmin system, cathepsin D, elastase, and lipase. The

study of plasmin system and lipase is well documented

(Albenzioet al., 2004a,2005a,2009b;Battaconeet al., 2005;

Caroprese et al., 2007; Chvarri et al., 1998; Chilliard et al.,

2003; Cortellino et al., 2006; Fantuz et al., 2001) whereas

cathepsins and elastase in small ruminant have received

attention recently (Albenzio et al., 2009b; Moatsou et al.,

2008; Santillo et al., 2009b).

Indigenous proteolytic enzymes are mainly associ-

ated to leukocyte cells: polymorphonuclear neutrophilic

leukocyte (PMNL), macrophages, lymphocytes which are

groupedtogetherwithmammary epithelial cells and iden-

tified assomatic cells (SC). Plasmin activity isunder control

of a complex enzymatic system in which one of the plas-

minogen activators results associated with somatic cells

(Politis et al., 1991); somatic cells contain lysosomes that

release active proteloytic enzymes i.e. elastase, cathep-

sin and collagenase (Kelly andMcSweeney, 2002). Several

authors have reported that an increase in bovine milk

somatic cell count (SCC) causes an increase in the amount

ofmilk proteolytic activitywhich in turn reduces the yield

and quality of cheese (Ali et al., 1980; Grandison and Ford,

1986; Verdi and Barbano, 1991). It is worth to note that

milk from small ruminants is characterized by different

levels of total somatic cells and distribution of leuko-

cyte cell type than bovine milk (Albenzio et al., 2004a,

2009b; Caroprese et al., 2007; Chen et al., 2010; Cuccuru

et al., 1997; Morgante et al., 1996). Recently Albenzio and

Caroprese (2011) reported thatpolymorphonuclear leuko-

cytes (PMNLs) represent the main population detected in

ewe milk with high somatic cell count (>1106 cells/mL)

andthat this leukocyteclasscouldbeuseful todifferentiate

ewe milk cell count being strictly responsible for the SCC

increase.

Changes in somatic cell count in ewes and goats milk

are associated with breed, parity, stage of lactation, type

of birth, estrus, diurnal, monthly and seasonal varia-

tion (Gonzalo et al., 2005, 2006; Raynal-Ljutovac et al.,

2007). When stage of lactation and level of SCC (


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M. Albenzio, A. Santillo / Small Ruminant Research 101 (2011) 3340 35

Lipoprotein lipase (LPL) has an important role in milk

production in themammary gland. Indigenous LPL cataly-

sesthe hydrolysis of triglycerides producingfree fattyacids

(FFA). Chandan et al. (1968) reported that lipase activity in

ovinemilkis about one-tenth and ingoatmilk isabout one-

third than that of bovine milk. The hydrolysis pattern of

ovinemilk fat byovine LPL exhibits a higher rate of hydrol-

ysis towards triglycerides containing medium-chain fatty

acids than towards those containing long chain fatty acids

(Chvarri et al., 1998). Lipolysis in caprine milk results in

the characteristic goat flavour due to the strong presence

of C6:0, C8:0, and C10:0 free fatty acids esterified on car-

bon 3, which are abundant in caprine milk fat (Ha and

Lindsay, 1993). Goat milk lipolysis and LPL activity vary

considerable and in parallel across goat breeds and geno-

types (Chilliardet al., 2003); Delacroix-Buchet et al. (1996)

report thatLPL activity ishigher ingoatmilkwith theweak

s1-CN FF genotype than in the goatmilk with the strongAA genotype.

4. Characteristics of cheese quality

The objective of cheese ripening is to convert the fresh

curd to one of the many cheese varieties with various

appearance, taste, flavour, texture, and functionality char-

acteristics.All theseare involved in thedefinitionof cheese

quality and are related to the intensity of the ripening pro-

cess in terms of proteolysis, lipolysis, and glycolysis.

Raw milk compositional and biochemical characteris-

tics, milk technological treatment and renneting process,

curd production, ripening of mature cheese represent a

multiplicityof factors that impact, directly or indirectly, on

the quality of dairy products. Each factor of this complex

system is affected by the activity of enzymes originated

frommilk (i.e. indigenous enzymes and microflora), coag-

ulants, and starter andnon starter microflora.

The coagulants used for cheesemaking hydrolyses

casein producing the initial breakdown products from

s- and -CNs at different rate depending on the coag-ulant used. Regarding indigenous proteolytic enzymes it

has been reported that plasmin acts on -CN and -CNleading to the formation of the polypeptides 12 3-CN andproteose-peptone, and-CN degradationproducts(Albenzio et al., 2010). However, the hydrolyses of princi-

pal caseins proceeds differently along with ripening time

with-CNproducts being releasedwithinthe first phaseofripeningwhereas thecleavageof-CNstarts less readily asan outcome of the different specificity of protolytic agents

towards caseins (Albenzioet al., 2010; Irigoyenet al., 2000;

Revilla et al., 2007).

Casein degradation and casein degradation products

represent an important index of cheese ripening and

describe, together with changes in proteolytic enzyme

activity, a complex pattern of events occurring during

cheese ripening. However, all these parameters are influ-

enced by several factors therefore they are not easily

related. Albenzio et al. (2004a) found that in ovine fresh

cheese curd the decrease of plasmin (PL) and plasmino-

gen derived (PG) activities coincided with an increase in

nonprotein nitrogen (NPN) suggesting that NPNmolecules

derived from CN hydrolysis may be involved in the

regulation of PLPG enzyme system. Furthermore, as

reported in previous studies (Albenzio et al., 2005b, 2010;

Santillo and Albenzio, 2008) changes in the formation of

-CN mainly derived from plasmin activity were not syn-chronized with the changes in PL activity in the cheese

during ripening.

Cheesemakingtechnology isoneofthemainfactorsable

to affect indigenous enzyme level and activity. In Canes-

trato pugliese ovine cheese, production protocol includes

heating the curd in hot whey: the rise of temperature can

promote syneresisandinactivationofheat-labileinhibitors

of PL and of PG activators (Albenzio et al., 2007). The influ-

ence of cheesemaking technology on PL and PG activities

in fresh acid cheeses Caprino and Chevre and in semi-hard

cheeses (Tronchetto, Caciotta, and Fiore Sardo) evidenced

that the acid curds had lower PL and PG derived activities

than semi-hard cheeses. Cortellino et al. (2006) ascribed

this result to the effect of the thermal inactivation of the

cooking step on PL inhibitors in semi-hard cheese. Heat-

ing of milk at 90 C (whey protein precipitation) removes

inhibitors of PG activators leading to higher levels of PL

activity in Cacioricotta goat cheese (Albenzio et al., 2006).

Salting of fresh curd is a further step able to influence

enzymatic activity in cheese during ripening; in fact, salt-

ingdepressestheactivityofmost of theenzymes in cheese,

including indigenous milk proteinases such as plasmin

(Sutherland,2003). Fox (2003) reportsthat hydrolysis of-CN is strongly inhibited by a NaCl content in the cheese of

5%. In Canestrato pugliese cheese from ewemilka salt con-

centration of about 4%was able to inhibit -CN hydrolysisas indicated by the limited accumulationof small peptides

ascribed to -CNs over 45d of ripening (Albenzio et al.,2004b, 2005b). Also lipolytic activity appears to be limited

at NaCl> 13g/kg of cheese in Idiazabal cheese made from

raw ewes milk and natural rennet (Njera et al., 1994).

Level of FFA in cheese are an outcome of the lipolytic pro-

cessoccurring inewe and goat cheeses and depends on the

length of ripening time. Traditional ewe and goat cheeses

are manufactured using lamb and kid rennet paste which

contains lipolytic enzymes that comprise pregastric and

gastric esterases responsible for the liberation of short and

mediumchain FFA in the cheesematrix (Jacob et al., 2010).

The balance of different lipases in rennet paste influences

thelipolytic pattern ofcheeseduring ripening,withamajor

content of short chain fatty acids in correspondence to

highcontent ofPGE (Collins et al., 2003). Furthermore,sev-

eral studies (Albenzio et al., 2001; Gobbetti and Di Cagno,

2003) have reported a higher level of FFA in cheeses made

from raw milk compared to pasteurized or thermal milk.

Besidemilk indigenous LPL such differences are attributed

to lipaseandesteraseactivities of themilkmicrofloraespe-

cially non starter lactic acid bacteria (NSLAB).

5. Cheese flavour

Flavour of cheese is determined by its taste and aroma

and results from the correct balance and concentration of

numerous sapid and aromatic compounds perceived dur-

ing cheese consumption. Proteolysis and lipolysis are of

great importance in the development of cheese flavour

and are ruled by the residual milk clotting enzyme, milk


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proteinase and lipase, proteolytic and lipolytic enzymes

from starter and non starter bacteria, and lipases asso-

ciated to certain coagulants (Collins et al., 2003; Visser,

1993). However, excessive proteolysis and lipolysis could

result in off-flavours because high concentrations of bit-

terpeptides andvolatileFFA, respectively, influencecheese

flavoureitherdirectlyor asprecursorsof other compounds

(Broadbent et al., 2002; Pinho et al., 2004). Theamino acids

liberatedin thecheesematrixduringsecondaryproteolysis

undergo further catabolic reactions which involve decar-

boxylation, deamination, transammination, desulfuration

leading to the production of compounds such as amines,

acids, and thiols. It is accepted that FFA, especially short

chain FFA, have a direct impactoncheeseflavour, FFAs also

act as precursor molecules which lead to the production of

other flavour compounds, such as methylketones, esters,

fatty acids lactones and alcohols (McSweeney and Sousa,

2000; Tziboula-Clarke, 2003). Diet is a main factor affect-

ing the odorof freshmilkbecause odorous substancesmay

be transferred to themilk (i) directly to inhaled air into the

blood and from there to the milk and (ii) by direct absorp-

tion from the digestive tract; and (iii) via rumen gases

to the blood and milk. Moio et al. (1996) identified two

sesquiterpenes in milk and cheese produced from sheep

fed on a natural pasture being these constituent of signifi-

cance for their role in determiningmilk and cheese flavour

and as chemicalmarkers of the milk used tomake cheese.

Luna et al. (2005) reported that the organoleptic charac-

teristics of cheeses made from CLA-enriched milk, from

ewes fed linseed supplements, did not differ from control

cheeses.

Processing milk with high SCC is associated with an

increase intheproteolysisrateanda modificationofcheese

proteolytic pattern (Coulon et al., 2004). The contribution

of indigenous proteinases in the development of cheese

flavour have a possible negative implication for the accu-

mulation of bitter peptides which are gradually formed

by further degradation of-CN compounds (Visser, 1993).Revilla et al. (2007) reported a lower overall acceptance of

ewe hard cheese made with high SCC milk compared to

medium and low SCC finding that the formerwas judge as

weaklybonded, very grainy, andcrumbly. On thecontrary,

Pirisi et al. (1996, 2000) did not found significant differ-

encesin sensorycharacteristicsand lipolyiscomparingewe

cheeses made from milk with low and high somatic cell

count. Accordingly, also in goat milkJaubert et al. (1996)

andMorganandGaspard (1999) founda minor effectof SCC

on the goatish flavour that is instead mainly influenced by

cheesemaking technology, in particular ripening methods.

Lamb rennet paste contains lipolytic enzymes which

initiate free fatty acid formation (Bustamante et al., 2000;

Santillo et al., 2007b; Virto et al., 2003) thus giving the

cheeses a sharp, piquant aroma; in particular butyric acid

contributes to the cheesy lipolyzed aroma (Pinho et al.,

2004). Agboola et al. (2004) investigated the formation

of bitter peptides, defined as peptides with a molecular

mass of 1656500g/mol, in semi hard ovine cheese: the

results showed that cheese made with Rhizomucor miehei

developedmore bitterpeptides compared to calf rennet. In

general, the coagulant also influences the development of

bitterness by an excessively high activity which depends

on its level and retention in cheese curd; in addition the

presence of certain starter i.e. lactococci have a propensity

to cause bitterness (Fox et al., 2000).

In ovine and caprine cheese the addition of starter and

probiotic cultures (Albenzio et al., 2001, 2010; Corbo et al.,

2001; Kalavrouzioti et al., 2005; Santillo and Albenzio,

2008; Santillo et al., 2007a, 2009a) has been associated

with an increased proteolysis and lipolysis. These cheeses

were tested for sensory attributesbya panel of non trained

consumers. Theresultshowedanabsenceofperceivedsen-

sory attributes inovinecheesewhereasflavourandgeneral

acceptance of caprine cheese had higher scores than the

control cheese.

High pressure treatmentof goatmilk destined to cheese

production (Saldo et al., 2003) had no negligible changes

on the volatile composition therefore pressure can be

regarded as a safe technology not producing unexpected

compounds inmilk and cheese.

6. Cheese rheology and texture

Cheese texture may be defined as a composite sen-

sory attribute resulting from a combination of physical

properties and perceived by the senses of sight, touch,

and hearing (Pinho et al., 2004). While these attributes

are manifested during cheese consumption, mechanical

properties of cheese are determined by the application

of a fixed stress or strain (i.e. compression, shearing,

or cutting) to a sample of cheese under defined exper-

imental conditions. These properties are related to the

composition, microstructure (i.e. the structural arrange-

ment of its components), the physico-chemical state of

its components, and itsmacrostructure, which reflects the

presence of heterogeneities such as curd granule junction,

cracks andfissures, level of fat coalescence, solid fat:liquid

ratio, degree of hydrolysis and hydration of the paraca-

seinmatrix, andlevel of intermolecularattraction between

paracasein molecules (Fox et al., 2000).

Manufacturing process isable to influence cheesestruc-

ture thus it is closely related to the rheological parameters

of cheese. In general, the rheological characteristics differ

markedly with the cheese variety and its age. The changes

occurred in the structural component of cheesematrix are

mediatedby theresidual rennet,microorganisms andtheir

enzymes and changes in mineral equilibria between the

serum andparacasein matrix. Chymosin, the primary pro-

teolytic agent hasbeen associatedwith softeningof cheese

texture via hydrolysis ofs1-I-CN (Albenzio et al., 2010).Semi-hard goat cheese manufactured using artisanal kid

rennet paste was found to have a slightly harder, crumbly

andgritty texture than cheesemade with commercial ren-

net due to the lower proteolysis observed and this was

reflected in less softening of the cheese mass (Fontecha

et al., 2006). Pecorino cheeses produced using traditional

rennet paste or rennet paste containing probiotic dis-

played different rheological parameters as a consequence

of the degree of casein breakdown observed during ripen-

ing(SantilloandAlbenzio,2008). Theuse of selectedstrains

of lactic acid bacteria for cheese production promotes ren-

netactivityby reducingmilkpH,aids theexpulsionofwhey

from the curd thus reducing the moisture content of the


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M. Albenzio, A. Santillo / Small Ruminant Research 101 (2011) 3340 37

cheese(Fox etal.,2000). Level ofpHalso playsan important

role in cheese texture: as the pHof cheese curds decreases,

there is a concomitant loss of colloidal calcium phosphate

fromthecasein submicelleswithaprogressivedissociation

of the submicelles into smaller casein aggregates at a pH

value below 5.5 (Lebecque et al., 2001). Upreti et al. (2006)

found that the disaggregation of caseinmicelles exposes a

larger surface area of proteins to proteinases and leads to

an increase in enzymesubstrate interaction. It has been

shown that high acidity, protein, and total solids contents

generallymake thecheeseharderand less easilydeformed

(Kehagias et al., 1995).

Park et al. (2007) and Revilla et al. (2007) reported

important changes in the textureof cheese frommilkwith

SCC over 2.5106 cells/mL: low WarnerBratzler Shear

Force (WBSF) values in cheese were related to the increase

in proteolysis and to the higher amounts of s1-I-CN.Chen et al. (2010) reported lower hardness and higher

springiness in semi soft goat cheese made frommilk with

SCC


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Biochemical Characteristics of Ewe and Goat Milk (2011)

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