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«Lars Wiking Faculty of Natural Resources and Agricultural Sciences Department of Food Science Uppsala Doctoral thesis Swedish University of ...»

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Xanthine dehydrogenase/oxidase is a redox enzyme containing molybdenum. The Mw of xanthine oxidase is 155 kDa and it accounts for about 8% of the protein in MFGM (Briley & Eisenthal, 1975). The best known function of the enzyme is the oxidation of hypoxanthine to xanthine and xanthine to uric acid. Furthermore, xantine oxidase can reduce NO3- to NO2-. The latter property is used in cheese manufacturing, where a small amount of nitrate is added because NO2- prevents Clostridia from growing. Recently, has been reported that aldehydes, naturally found in milk, can accelerate the oxidation in raw milk through the xanthine oxidase enzyme system (Steffensen, Andersen, Nielsen, 2002). Xanthine oxidase is thought to be a peripheral membrane protein, meaning that it is not a membrane anchor and is thereby easily released from the MFGM. During cooling, xanthine dehydrogenase is thus released into the milk serum where it is activated (Bhavadasan & Ganguli, 1980).

Butyrophilin (PAS 5) comprises over 40% by weight of the MFGM proteins. Its Mw is 67 kDa and contains approx. 5% carbohydrate. Butyrophilin is only expressed on the apical plasma membrane of secretory cells in the mammary tissue, and butyrophilin is a transmembrane protein (Jack & Mather, 1990). The Cterminal of butyrophilin interacts with xanthine oxidase (Figure 2) supported by disulfide bonds between the proteins and thereby stabilises the MFGM (Mather & Keenan, 1998). Mondy and Keenan (1993) reported that butyrophilin and xanthine oxidase are present in the MFGM in constant molar proportions (4:1) through lactation. Later, Ye et al. (2002) confirmed the constant ratio except that the ratio was 3:1. Butyrophilin and xanthine oxidase are tightly attached to fatty acids with palmitic, stearic and oleic acids as the predominant protein-bound fatty acids (Keenan & Heid, 1982).

PAS-6 and PAS-7 are abbreviations for Periodic Acid Schiff 6 and 7, respectively.

Their Mw ranges from 43 kDa to 53 kDa (Mather, 2000). The amino sequences of PAS 6 and PAS 7 are identical, but vary in glycosylation. The actual glycosylation

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When the MFG is expelled through the apical membrane, γ-glutamyl transpeptidase is loosely included in the MFGM. However, in cold-stored milk 74% of the total activity of γ-glutamyl transpeptidase is in the skim milk (Baumrucker, 1979). The enzyme consists of two subunits with Mw of 57 kDa and

25.5 kDa, respectively (Baumrucker, 1980). Furthermore, γ-glutamyl transpeptidase is involved in the amino acid uptake for milk protein synthesis (Johnston et al. 2004).

Triglycerides are the major fraction of neutral lipids in the MFGM. However, most of this is believed to originate from contamination (from the core of the MFG) during isolation of the membrane (Walstra 1974 and 1985). Whole milk contains 308 to 606 mg cholesterol /100 g fat (Jensen, 2002). The majority is located in the MFGM. Walstra et al. (1999) reported the cholesterol content in the MFGM to be 0,2 mg/m2. However, the proportion of cholesterol decreases through lactation (Bitman & Wood, 1990). Mono- and diglycerides, FFA and glycospringolipids are also present in the MFGM. The latter of the four consists of neutral glycolipids and gangliosides. The quantity of gangliosides is about 8µg/mg membrane protein and the composition is identical to apical plasma membranes of the secretory cells in the mammary gland (Jensen, 2002).

In bovine milk about 60% of the phospholipids is associated in MFGM while the rest is located in the skim milk phase (Patton & Keenan, 1975). The quantity of phospholipids in milk declines through lactation and the decline is larger than the decrease in total milk fat through lactation (Bitman & Wood, 1990). The most abundant phospholipids are the zwitterionic; phosphatidylcholine, phosphatidylethanolamine and sphingomyelin, while the anionic forms phosphatidylserine and phosphatidylinositol are present in lower amounts. The MGFM phospholipids contain high levels of palmetic and oleic acid, while the short and medium-chain fatty acids are present in very low levels (Mcpherson & Kitchen, 1983). The fatty acid composition in the core milk fat can be changed through the feeding of cows. Simultaneously, the composition of the phospholipids is changed. Smith, Bianco and Dunkley (1977) found that feeding a supplement rich in linoleic acid increases the unsaturation of the phospholipids in outer and inner milk fat globule membranes. However, this unsaturation was less than that of the core lipids. Palmquist and Schanbacher (1991) observed that by feeding palmitic acid to the cow, it is possible to increase the saturation of the lipids in the membrane.

Phospholipids form the basic bilayer in biological membranes in which the nonpolar tails are arranged side-by-side and turn towards the lipids. The polar head groups are orientated towards the aqueous environment. A suggestion of the proposed structure of the MFGM is shown in Figure 2. There is a layer of highmelting triglycerides surrounding the core fat. Xanthine oxidase is assumed to be a peripheral membrane protein since it does not containing a long sequence of 14 nonpolar amino acids to function as membrane anchor (Mather & Keenan, 1998).

However, xanthine oxidase is probably associated with the inner membrane (Mather & Keenan, 1998). Butyrophilin is an integral membrane protein and therefore an important factor in stabilising the MFGM.

Figure 2. Structure of the milk fat globule membrane.

(Michalski et al., 2002). Reproduced with permission from Elsevier.

Lipolysis in milk Lipase Lipoprotein lipase (LPL) is the enzyme mainly responsible for lipolysis in raw milk. It originates from the mammary gland, where it is involved in the uptake of blood lipids for milk synthesis. The enzyme is active in lipid-water interfaces. Its optimum temperature is 33°C, and pH optimum is about 8.5. It is a relatively heat labile enzyme which is mostly inactivated by a high temperature-short time heat treatment. In milk, LPL is mainly associated with the casein micells (Hohe, Dimick & Kilara. 1985). LPL is brought into contact with the triglycerides when the MFGM is disrupted and casein coats the formed lipid-water interface. The enzyme is activated by apo-lipoprotein CII from the blood which assists LPL to bind onto the fat globule (Bengtsson & Olivecrona, 1982). In spite of the high amount of LPL in milk, lipolysis is limited since milk fat is protected by the membrane and raw milk is normally stored at temperatures far below the optimum temperature of LPL. Furthermore, the products of the hydrolyses of the triglycerides, the FFA, inhibit the enzyme presumably due to that the FFA binding to the LPL. Furthermore, the proteose-peptone component 3 is found to inhibit LPL (Cartier, Chilliard & Paquet, 1990; Girardet et al. 1993).

Several investigations have shown that the activity of LPL in whole milk is not correlated to FFA content in raw milk (Salih & Anderson, 1979; Bachman & 15 Wilcox, 1990a; Cartier & Chillard, 1990). On the other hand, other studies show that the activity of lipoprotein lipase in the cream fraction is related to the level of lipolysis (Ahrne & Björck, 1985; Bachman & Wilcox, 1990; Cartier & Chillard, 1990). Consequently, the formation of FFA is assumed to be dependent on MFG susceptibility to action of lipases. LPL preferentially hydrolyses fatty acids in position sn-1 and sn-3. The fatty acids placed with high frequencies on position sn-1 and sn-3 are C4, C6, C18 and C18:1 (Walstra & Jennes, 1984; Jensen, 2002).

This is in agreement with the recent report by Ouattara et al. (2004) who demonstrated that C4, C6 and C18:1 were the most freqent free fatty acid in a mixture of raw and pasteurised milk stored at 4 °C for 48 hours. Lipases synthesized by bacteria or yeast can also be present in milk. However, if milk is properly stored and has an acceptable hygienic quality, microbial lipases are not an important factor for lipolysis until after several days of storage.

The classic division of lipolysis in milk is between spontaneous and induced lipolysis (Jellema, 1986). The factors affecting spontaneous lipolysis include milking frequencies, udder health and stage of lactation. Induced lipolysis is caused by homogenisation, pumping and temperature fluctuations.

Lipolytic rancid flavour The rancid flavour developing from lipolysis is often described as gouty or soapy.

Several studies have tried to find the relationship between the rancid off-flavour and the level of FFA in milk. As shown in Table 4, the literature based on sensory panel tests indicates no completely clear relationship between the level of FFA and flavour threshold. However, the risk of a rancid off-flavour will always

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increase with an increase in FFA concentration. Shipe, Senyk & Fountain (1980) found that the correlation coefficient between ADV (acid degree value) and rancid flavour score was r2=0.67. In contrast, Duncan, Christen & Penfield (1991) reported a poor correlation (r2=0.02) between the level of FFA (similar to acid degree value) and rancidity flavour score. Recently, Gonzalez-Cordova & VallejoCordoba (2004) found a high correlation between short-chain FFA determined quantitatively by solid phase microextraction-GC and sensory scores by using a multiple regression analysis. In addition, they also found a significant correlation (r2=0.84) between level of FFA and sensory score. The advantages and 16 disadvantages of the analytical method for determination of the level of FFA are discussed further in the material and method section.

The development of a rancid flavour in milk is greatly affected by the composition of FFA. It is mainly the fatty acids with chain length from 4 to 12, which contribute to the rancid flavour. Duncan & Christen (1991) observed that the flavour threshold in milk for added C4 is 0.20 µmol/ml compared with 0.55 µmol/ml for C18:1. Likewise, Urbach, Stark & Forss (1972) reported that a concentration of 3 ppm added C4 is the flavour threshold in butter, while the threshold for C14 is 100 ppm. Culturing or acidification of the milk increase the appearance of rancid flavour at the same level of FFA, presumably as a result of changing the ratio of fatty acids to fatty acid salt (Tuckey & Stadhouders, 1967).

In a Canadian study, rancid off-flavour was the second most appearing offflavour, after feed-transmitted off-flavour in farm bulk tank milk (Mounchili et al.


Changes induced to milk fat globules during different treatments Influence of mechanical treatment on MFG stability It has been suggested that of the final FFA level in pasteurised milk around 60is due to lipolysis occurring during milking and milk transfer to the bulk tank (Anderson, 1983). Mechanical treatments of the milk such as pumping and stirring subject MFG to physical stress. Higher flow velocities during pumping in pipes result in greater friction in the liquid itself and between the liquid and the pipe wall. These relative differences in flow velocity perpendicular to the flow direction are called shear rates. The shear rate depends on the diameter of the pipe and the flow velocity. The presence of air, the temperature of the milk and fat content affect the stability of the MFG during mechanical treatments of milk.

In milking systems, the milk is mixed with air, especially when air is used as a transport medium for the milk. The stability of the MFG is lowered by mixing with air or any other gas during pumping or agitation of the milk. The contact between a MFG and an air bubble results in rupturing of the MFG, since membrane material and part of the core fat will spread over the air/milk plasma interface and will be released into the milk plasma when air bubbles collapse or coalesce (Evers, 2004). Needs, Anderson & Morant (1986) reported that using a claw piece requiring high air bleed instead of a conventional claw increased FFA level by 21 %. Similar results were found by O´Brien, O´Callaghan & Dillon (1998) and Rasmussen et al. (unpublished results, 2005).

Pumping of cream is usually conducted at lower flow rates compared with pumping of milk. Studies have suggested that the stability of the MFG decreases linearly with increasing fat content in milk/cream (Hinrichs & Kessler, 1997;

Hinrichs, 1998). This is ascribed to the increased friction between fat globules.

The milk temperature is also a very important factor when milk is exposed to mechanical treatments. Several studies have reported that the maximum 17 accumulation of FFA upon agitation is at a temperature of ~15 °C and again after ~30°C, with low formation of FFA between 20-30 °C (Fitz-Gerald, 1974; Deeth & Fitz-Gerald, 1977; Bhavadasan, Abraham & Ganguli, 1981; Hisserich & Reuter, 1984). At low temperatures the milk fat is more resistant to mechanical stress.

Homogenisation of milk can only be successful at temperatures above 40°C. The effect of temperature on MFG stability is due to crystallization of lipids. One minor factor is that the temperature affects the activity of LPL.

Crystallisation of fat The most common process during the manufacture of dairy products is cooling.

The crystallisation point of milk fat is broad due to a large variety of triglycerides.

The crystallisation process of milk fat includes two steps; nucleation and crystal growth.

Crystallisation starts in a supercooled liquid with the formation of submicroscopic crystal nuclei. Nucleation is often heterogenous and takes place at the surface of very small particles. These particles are called catalytic impurities. When a fat crystal has been formed it can act as a catalytic impurity for other triglycerides. In anhydrous fat, it requires a supercooling of only a few degrees centigrade to form enough catalytic impurities to induce crystallisation. In milk, however, it is different since the fat is divided into many globules and in every single globule one nucleus must be formed. The crystallisation rate increases with increasing lipolysis of the fat and it is therefore suggested that crystals of monoglycerides are the predominant catalytic impurities in milk fat (Walstra and van Beresteyn, 1975).The MFG size affects the necessary supercooling to start nucleation, i.e.

deeper supercooling is required in small globules (Walstra & Beresteyn, 1975) The growth of crystals in milk is very slow as the many competing molecules try to fit into a vacant site in the crystal network (lattice). Often, incorrect molecules occupy the vacant site for a while before they diffuse out of the lattice, and make place for a proper molecule. The order of the crystal network has to be very systematic and precise.

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