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The Structure of Milk: Implications For Sampling and Storage
The Structure of Milk: Implications For Sampling and Storage
THOMAS W. KEENA N
STUART PATTO N
H A N D B O O K O F MIL K COMPOSITIO N
Copyright © 199 5 b y Academi c Press , Inc.
All righ u reserved . N o reproductio n withou t permission .
6 Thoma s W. Keena n and Stuart Patto n
A. Droplet Formation
B. Growt h of Drop/ets
D. Significance of Crescent s
A. Globule Size
Milk lipi d globule s o f specie s examine d t o date fal l int o thre e overlappin g
size distributions : smal l wit h diameter s centere d belo w 1 ^im, intermediat e
with diameter s i n th e 3 t o 5 [A m range, an d larg e globule s wit h a mea n
diameter o f abou t 8 t o 1 0 [im . Som e o f th e latte r approac h 2 0 [i m an d i t
is fel t tha t thi s group , fo r th e mos t part , i s forme d b y postsecretio n
merging o f globules . Thus , mil k fa t globule s tha t ar e mos t typica l a s
secretory product s belon g t o th e tw o smalle r groups . However , a surpris -
ingly larg e proportio n o f th e tota l globul e population , 7 0 t o 90 % i n th e
bovine an d human , lie s i n th e first grou p belo w 1 |im i n diameter . Whil e
2. Th e Structur e o f Mil k 1 5
Riiegg and Blan c (1981 ) estimat e tha t th e lipi d globul e surfac e are a i n 1 ml
of matur e huma n mil k i s 500 cm^ . I n a liter o f milk , thi s would b e 500,00 0
cm^ o f surfac e o r roughl y th e floor spac e i n a roo m 2 3 ft^ . Whethe r on e
thinks o f mil k i n term s o f processin g an d storag e effect s o r digestio n an d
behavior i n th e gut , thi s i s a larg e amoun t o f surface . W e ca n assum e tha t
the surfac e are a o f lipi d globule s i n mil k i s roughl y equivalen t t o tha t o f
16 Thoma s W. Keena n and Stuart Patto n
B. Gross Composition
TABLE I
Gross Composition of Cow an d Human Mill < Lipid Globule Membrane Preparation s
Protein weight % 25 t o 6 0 —
Total lipid s mg/mg protei n 0.5 t o 1. 1 1.46
Phospholipids mg/mg protei n 0.13 t o 0.3 4 0.35
Neutral lipid s mg/mg protei n 0.25 t o 0.8 8 1.1
Glycosphingolipids'^ [ig/mg protei n 13 32
Hexoses ^Ag/mg protei n 108 45
Hexosamines Hg/mg protei n 66 44
Sialic acid s |Ag/mg protei n 20 18
Glycosaminoglycans Hg/mg protei n 0.1 -
RNA Hg/mg protei n 20 15
C. Lipid Composition
1. Neutral Lipids
Values reporte d fo r th e amount s o f mos t o f th e lipi d classe s o f huma n
MLGM fal l withi n th e rang e o f value s reporte d fo r co w MLG M (Tabl e II) .
In membrane s fro m bot h sources , triacylglycerol s ar e th e mos t abundan t
lipid class . Since preparativ e metho d ha s a majo r influenc e o n th e amoun t
of triacylglycero l associate d wit h MLGM , i t i s likel y tha t som e o f th e
triacylglycerols originat e fro m th e cor e lipid s an d adsor b ont o o r partitio n
into th e membran e material . Fatt y aci d compositio n o f MLGM-associate d
triacylglycerols differ s fro m tha t o f mil k fa t i n tha t MLG M triacylgly -
cerols contai n considerabl y highe r proportion s o f long-chain , saturate d
fatty acid s (principall y palmitat e an d stearate ) (Kitchen , 1977) . Vasi c an d
DeMan (1966 ) an d Bracc o et al. (1972 ) foun d tha t whe n fa t globule s wer e
destabilized a t temperature s abov e 37°C , isolated MLG M wa s no t enriche d
in high-meltin g triacylglycerols . Walstr a (1974 ) suggeste d tha t thes e high -
melting triacylglycerol s ma y b e derive d fro m fa t crystal s whic h "contami -
nate'* th e membran e durin g th e coolin g an d churnin g process . Result s
from microelectrophoreti c characterizatio n o f lipi d globule s le d Newma n
and Harriso n (1973 ) t o conclud e tha t th e oute r surfac e o f th e MLG M
contains littl e neutra l lipid . Trac e t o substantia l quantitie s o f mono - an d
diacylglycerols usuall y ar e foun d i n MLG M lipids . Whethe r thes e partia l
glycericdes ar e tru e constituent s o f membrane s o r ar e product s o f lipolyti c
degradation o f triacylglycerol s o r phosphoglyceride s i s no t known . T h e
amounts o f unesterifie d fatt y acid s foun d i n MLG M preparations , a t leas t
from cow , var y widely . Thi s variatio n ma y b e du e t o variatio n i n lipolyti c
activity. Sterol s an d stero l ester s invariabl y ar e foun d i n MLG M lipids ;
however, ther e i s extensive variatio n i n stero l conten t judged fro m value s
reported fo r co w MLGM . Som e o f thi s variatio n ma y b e th e resul t o f
preparative method-induce d differentia l partitionin g o f sterol s betwee n
core an d membran e lipid s (discusse d i n Keena n et a/., 1988) . Cholestero l
is presen t i n lipi d droplet s befor e secretio n a s mil k lipi d globules , bu t it s
distribution betwee n th e cor e lipid s an d materia l o f th e surfac e coa t i s
unknown (Dylewsk i et al., 1984) . Cholesterol i s a known an d abundan t lipi d
constituent o f plasm a membrane , fro m mammar y glan d (Keena n et ai,
1970; Kann o et ai, 1987) , a s wel l a s othe r tissue s (reviewe d i n Va n Meer ,
1989). An ultrastructura l approach , i n whic h cholesterol-filipi n complexe s
were visualize d i n freeze-fractur e replicas , provide d evidenc e fo r th e
presence o f cholestero l bot h i n o r a t th e surfac e o f cor e lipids , an d i n th e
MLGM i n intac t mil k lipi d globule s (Martin , 1989) . This observatio n doe s
not rul e ou t partitionin g o f cholesterol betwee n membran e an d cor e lipid s
before globule s ar e harveste d an d destabilized . I n MLG M fro m bot h cow s
and humans , stero l ester s accoun t fo r a smal l proportion , 10 % o r less , o f
the total sterols. Fat globules, but no t necessaril y MLGM , from huma n mil k
contain a muc h highe r amoun t o f cholestero l tha n d o thos e i n co w mil k
22 Thomas W. Keena n and Stuart Patto n
TABLE I I
Lipid Composition of Cow an d Human Mill c Lipid Globule Membrane Preparation s
% of total lipi d
Triacylglycerols 62 5 8
Diacylglycerols 98
Monoacylglycerols Trace 0. 6
Sterols 0.2 t o 2 0. 7
Sterol ester s 0.1 t o 0. 3 Trac e
Unesterified fatt y acid s 0.6 t o 6 7. 3
Hydrocarbons 1.2 Trac e
Phospholipids 26 t o 3 1 2 3
% of tota l phospholipi d
Sphingomyelin 22 2 6
Phosphatidyl cholin e 36 3 0
Phosphatidyl ethanolamin e 27 3 7
Phosphatidyl inosito l 11 5
Phosphatidyl serin e 41
Lysophosphatidyl cholin e 22
(Braco et ai, 1972) . Cholesterol i s the major sterol in human an d cow milks,
accounting fo r ove r 90 % o f th e tota l stero l fraction . Abou t 1 7 differen t
sterols have been isolate d fro m co w milk ; thos e whic h hav e been identifie d
include 7-dehydrocholesterol , campesterol , stigmasterol , an d ^-sitostero l
(reviewed i n Blanc, 1979) . I n addition t o cholesterol, 7-dehydrocholestero l
and phytosterol s hav e bee n foun d i n huma n milk . Whic h o f thes e sterol s
are i n MLG M ha s ye t t o b e determine d wit h eithe r species . Squalene , th e
abundant hydrocarbon o f cow and human mil k fat (Bracco etai, 1972) , has
been identifie d a s a constituen t o f co w MLG M (Thompso n et al, 1961) .
P-Carotene als o i s presen t i n th e hydrocarbo n fractio n o f co w MLG M
(Thompson et a/., 1961) , but mos t of th e carotenoid o f th e globul e appear s
to b e i n th e cor e lipi d (Patto n et al., 1980) . Carotene s als o ar e associate d
with huma n mil k lipi d globules , bu t th e distributio n betwee n cor e lipid s
and th e MLG M ha s ye t t o b e determined .
2. Phospholipids
3. Glycosphingolipids
Glycosphingolipids, relativel y mino r constituents o f th e MLG M (Tabl e
I), hav e bee n th e subjec t o f a numbe r o f investigation s ove r th e pas t sev -
eral years . Thi s attentio n ha s bee n du e t o th e recognitio n tha t certai n
glycosphingolipids an d product s o f glycosphingolipi d catabolis m hav e
24 Thoma s W. Keena n and Stuart Patto n
D. Protein Composition
HB
7 » - .... .
[ ^m ^ ^ .._ , -20 5
-** s i
^ ^ ^ WKM H ^ ^ ^ W JNHM K ^ ^ ^ ^ T
i
"^ -11 - 9 76
n H I 11 .u
M1 mi ^^ ^"1 -66
^ ^ ^ SJM ^ <ll««'^"''' » *'•'«?»» '
mm flK M&^ Mt t
Figure 4 A n SDS gel showing polymorphism o f the bovine milk lipid globule mucin, PAS-I,
among fiv e animal s (i n brackets) . Not e variabl e numbe r an d mobilit y o f bands . Positio n o f
molecular weight references i s indicated in kDa at left. The gel contained 6 % acrylamide and
was stained with silver reagents. Each of the five samples were 1 0 jig of total globule protein.
3. Lectin Binding
TABLE IV
Enzymatic Activities Detecte d in Cow an d Human Mil k Lipi d Globule Membran e
Preparations
''Common or trivial name of enzyme i s followed b y the Enzym e Commission (EC ) referenc e
number.
^Letter indicate s tha t enzym e ha s bee n reporte d i n MLG M o f tha t species , an d key s th e
reference: A , reviewe d i n Keena n et al. (1988) ; B , Shrive r et al. (1989 ) foun d acetyl-Co A
carboxylase to be present in enzymatically inaaive form; C, Martel-Pradal and Got (1972); D,
Zikakis^/fl/. (1976) ; E. Burder ^^a/. (1978) ; F, Martel etal (1973) ; G, Martel and Got (1976a);
H, Parod i et al. (1984) foun d enzyme s o f synthesi s o f dolicho l monophosphomannos e an d
dolichol monophosphoglucose , a s well as those involved i n transfer of glycosy l residu e fro m
these dolicho l derivativ e t o dolichol diphosphooligosaccharides .
36 Thoma s W. Keena n and Stuart Patto n
1. Cooling
creaming i s greatl y delaye d i n goat' s milk . Whil e a crea m laye r wil l for m
within 1 5 o r 2 0 mi n o n cow' s milk , i t require s hour s o f holdin g fo r goat' s
milk. Thi s i s no t s o muc h du e t o th e smalle r siz e o f goa t globules , whic h
is true, as it is due t o slowness of th e globule s i n clumping together . Fo r thi s
reason, goat milk is said to be naturally homogenized . T h e earlie r literatur e
on creamin g o f cow milk ha s been reviewe d extensivel y b y Brunner (1965) .
No doub t ther e ar e man y temperature-sensitiv e adsorbtion -
desorbtion phenomeno n i n additio n t o agglutini n bindin g transpirin g i n
milk. Anothe r facto r relate d t o thi s i s the progressiv e crystallizatio n o f th e
glycerides i n th e globul e cor e an d o f th e lipid s i n th e MLG M a s mil k cools .
We expec t thi s t o chang e th e positio n an d configuratio n o f som e mem -
brane components : i n som e cases , irreversibly . Moreover , w e expec t a n
accompanying los s o f membran e fluidity i f suc h fluidity exists .
As cow milk is held a t 0-5°C , th e amount o f lipid recovere d i n th e ski m
milk o n centrifuga l separatio n increase s graduall y ove r 4 8 h r (Patto n et a/.,
1980b). Thi s lipi d wa s measure d b y solven t extractio n an d weighing . I t i s
most likel y membran e derive d an d indicate s th e sluffin g o f MLGM . I n thi s
connection, i t i s o f interes t tha t ski m mil k o f lowes t cholestero l conten t
should resul t b y separatin g th e freshes t mil k possible .
3, Oxidized Flavor
4. Freezing
5. Heating
will also remove membran e fro m mil k lipid globule s (Patto n et ai, 1986) .
Methods of preparin g MLG M using surfactants ar e discussed unde r Sec-
tion VI, A. Highe r concentrations o f surfactants, especially when coupled
with heat treatment, cause both release of th e membrane and dissociation
of it s components . Th e powerfu l detergent , SDS , i s use d t o completel y
dissociate protein s fro m membran e t o facilitat e thei r electrophoretri c
analysis.
1. Churning
No doubt the production of butter happened by accident thousands of
years ago when some beast of burden carried a container of milk over some
distance. Fundamentally , agitatio n i s all tha t is needed, an d i f i t is main-
tained long enough, butter will be produced. Th e proces s is also aided by
the incorporatio n o f air , hig h fa t content, suc h a s in heav y cream , an d a
suitable temperature. When air bubbles are suspended i n a liquid, such as
milk or cream, the y will tend t o take u p surface activ e material s i n order
to lower their free surface energy and become physically more stable. One
of th e substance s tha t bind s t o th e ai r cell s unde r thes e condition s i s
MLGM. This tends to denude lipi d globule s and expose thei r underlyin g
triacylglycerols. A t the churning temperatur e (approximatel y 12''C ) these
patches o f glyceride s ar e semisoli d (sticky ) an d ten d t o adher e t o on e
another, especiall y unde r th e rigorou s physica l agitatio n o f th e churn .
Eventually th e growin g globul e aggregate s destabiliz e th e air cells (foam )
and, with continued churning, these aggregates become particles of butter.
Much of th e membrane , bu t not all, goes into the buttermilk. Membran e
is stil l retaine d b y som e o f th e fa t globule s i n th e butte r a s see n i n
freeze-fracture replica s in the electron microscope (W. Buchheim, personal
communication). I t i s fel t tha t th e MLG M remainin g i n th e butte r help s
with th e incorporatio n o f moistur e durin g th e workin g proces s an d th e
creation o f a product tha t feel s smoot h o n th e tongue .
2. Th e Structur e o f Mil k 4 3
2. Homogenization
The discover y tha t homogenizatio n stabilize d th e suspensio n o f fa t i n
milk, mad e th e mil k tast e creamier, increase d milk' s resistance t o oxidize d
flavor, an d lowere d th e cur d tensio n mad e fo r rapi d adoptio n o f th e
process. Homogenizatio n i s effecte d b y pumpin g mil k a t hig h pressur e
through narro w orifice s a t temperatures approximatin g thos e fo r pasteur -
ization (65-80°C) . Thi s produce s drasti c turbulen t an d cavitationa l force s
which physicall y disintegrat e th e globules , particularl y th e large r ones ,
leading t o a reduction i n thei r mea n diamete r fro m 3 or 4 [A m to less tha n
1 [im . Th e expose d ne w triacylglycero l surface s adsor b mil k proteins ,
particularly casei n micelles . Abou t 30 % of th e casein i n homogenize d mil k
is associate d wit h th e lipi d globules . Th e resultin g globul e suspensio n i s
probably stabilized in two ways. The adsorbe d protei n increases the densit y
of th e globules , thu s overcomin g thei r tendenc y t o rise , an d th e negativ e
charge o f adsorbe d casei n micelle s probabl y make s th e globule s mor e
self-repellent. I t is also possible that such clumping factor s as agglutinin ar e
denatured i n th e homogenizing . I n an y event, th e norma l tendenc y o f th e
globules t o clump seem s t o be destroyed . However , a study (Keena n et ai,
1983) has made it clear that a large proportion o f globule s in homogenize d
milk stil l retai n membran e material , bot h protei n an d lipid , an d tha t uni t
(normal biological ) membran e structur e ca n b e observe d o n the m i n th e
electron microscope .
Acknowledgements
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2. Th e Structur e o f Mil k 4 9
B. Particulat e Constituent s
in Huma n an d Bovin e Milk s
ROBERT G. JENSEN
BERNARD BLANC
STUART PATTO N
I. Introductio n
H A N D B O O K O F MIL K COMPOSITIO N
Copyright ® 199 5 b y Academi c Press , inc.
All righ u reserved . N o reproductio n withou t permission .