- Email: [email protected]
Modifying milk composition through forage
Animal Feed Science and Technology 131 (2006) 207–225
Review
Modifying milk composition through forage A. Elgersma a,∗ , S. Tamminga b , G. Ellen c a
Wageningen University, Crop and Weed Ecology Group, Graduate School of Production Ecology and Resource Conservation (PE&RC), Haarweg 333, 6709 RZ Wageningen, The Netherlands b Wageningen University, Animal Sciences Group, Graduate School Wageningen Institute for Animal Sciences (WIAS), Marijkeweg 40, 6709 PG Wageningen, The Netherlands c NIZO Food Research, P.O. Box 20, 6710 BA Ede, The Netherlands Accepted 16 June 2006
Abstract The fatty acid (FA) composition of cows milk has become less favorable to human health in the last four decades due to changed feeding and management practices, notably higher proportions of concentrates and silages in diets with less grazing. Essential FA and conjugated linoleic acid (CLA) concentrations have generally declined and, with more ‘low-fat’ dairy products, human intake of these FA has declined even further since ruminant food products are the main source of human CLA intake. Changing societal drivers and consumer demands require dairy production systems that provide food products through sustainable production systems. Milk FA were examined in milk produced in different regions of the world, in the different seasons of the year, and under different feeding systems. FA levels were examined in forages, concentrates and milk. Milk from cows fed fresh green forage, especially those grazing grass, had a much higher unsaturated:saturated FA proportion, with more polyunsaturated FA and more CLA (in particular C18:2 cis-9, trans-11), than milk from silage-fed cows. Farmers from some dairy cooperatives in The Netherlands that produce milk from grazed grass now receive a premium payment in addition to the base milk price, so that primary producers can benefit from the higher market value at the end of the production chain. © 2006 Elsevier B.V. All rights reserved. Keywords: Forage; Silage; Feeding system; Seasonal change; Milk fatty acids
Abbreviations: CLA, conjugated linoleic acid; DM, dry matter; FA, fatty acids; LDL, low density lipoprotein; MUFA, monounsaturated FA; PUFA, polyunsaturated FA; UFA, unsaturated FA ∗ Corresponding author. Tel.: +31 317 483523; fax: +31 317 485572. E-mail address: [email protected] (A. Elgersma). 0377-8401/$ – see front matter © 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.anifeedsci.2006.06.012
208
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
Contents 1. 2. 3. 4.
5. 6.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Lipids in plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Fatty acid conversions in the rumen and mammary gland . . . . . . . . . . . . . . . . . . . . . . . . . . . Lipids in milk . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Seasonal effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Regional, farming system and feeding system effects . . . . . . . . . . . . . . . . . . . . . . . . 4.3. Animal and breed effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Trends and future perspectives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
208 209 211 212 212 213 217 220 222 222
1. Introduction Changing societal drivers (e.g., landscape values, animal welfare) and consumer demands (e.g., tasty/healthy products) require systems that provide desired human foods produced through sustainable production processes. High-fat humen diets, especially those rich in saturated fats, are often claimed to have detrimental effects on cardiovascular disease risk factors such as blood low density lipoprotein (LDL) cholesterol (Ascherio et al., 1996; Williams, 2000). Dairy products contribute 15–20% of human intake of total fat, 25–33% of saturated fat and about 15% of dietary cholesterol in the USA (Havel, 1997). At present, about 2% of total fatty acids (FA) in milk are polyunsaturated (PUFA) and about 70% are saturated, but less than 40% of saturated FA are in categories considered to be less healthy. These values can be modified by changing the animal diets (Tamminga, 2001; Kennelly, 2001; Chilliard et al., 2001), and it is thought that lauric acid (C12:0), but especially myristic (C14:0) and palmitic (C16:0) acid, raise total and LDL cholesterol, whereas stearic acid (C18:0) is neutral relative to the monounsaturated fatty acid (MUFA) oleic acid (C18:1) in animal fats (Grundy and Vega, 1998). Cardiovascular risk might be reduced by lowering intake of undesirable saturated FA and/or by making alterations in the FA profile of the fat consumed. Increasing the concentration of desired FA in ruminant products is receiving current attention. The main n−3 FA in milk is ␣-linolenic acid (C18:3 cis-9, cis-12, cis-15), and another category of PUFA is conjugated linoleic acid (CLA), the main isomer in milk being rumenic acid (C18:2 cis-9, trans-11). The MUFA in milk consist mainly of C18:1 cis-9 (oleic acid) and also C18:1 trans-11 (vaccenic acid). Rumenic and vaccenic acids are both trans-11 FA produced by rumen microorganisms and are unique to ruminant fats. Rumenic acid has been associated with anticarcenogenic properties in rats (Corl et al., 2003; Ip et al., 1999) and possibly in humans (Aro et al., 2000; Belury, 2002). Other potential beneficial effects of CLA for human health were mentioned, but more work is needed to elucidate the safety and efficacy of isomers and their required doses (Belury, 2002). Ingested vaccenic acid can be converted into rumenic acid in mammals, including humans (Salminen et al., 1998; Santora et al., 2000). Turpeinen et al. (2002) estimated that, on average, humans endogenously convert 19% of dietary vaccenic acid into rumenic acid. Banni et al. (2001)
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
209
demonstrated that feeding vaccenic acid to rats, at 2% of the diet, not only increased tissue concentrations of rumenic acid, but also had a protective effect against development of mammary tumours, a similar effect to that later reported by Lock et al. (2004). This implies that, when calculating the dietary intake of rumenic acid, it is reasonable to add 20% of the vaccenic acid in the diet. The CLA contents in dairy product fats are comparable to those of the milk fat from which these products are obtained (Lavillonni`ere et al., 1998; Dhiman et al., 1999b). As milk FA composition is mainly determined by feed composition (i.e., the FA composition of the feed (Khanal and Olson, 2004), and feeding strategy (Tamminga, 2001)), effects of forage, feed and feeding systems will be discussed.
2. Lipids in plants Dairy cow diets are usually composed of a mix of fresh forages, mainly leaf blades, conserved forages (i.e., herbage leaf blades and also stems in spring; seeds and stems in case of forage maize) and concentrates (i.e., plant seeds). Diet composition of dairy cattle differs greatly among seasons and regions of the world. Some information is available about the lipid concentration, and its FA profile, of forages and the factors influencing them. The lipid fraction in leaves of herbs and grasses ranges from 30 to 100 g/kg DM, much of which is contributed by chloroplast lipids (Bauchart et al., 1984). Sources of variation in lipid concentration are plant species, growth stage, temperature and light intensity (Hawke, 1973), but there are five major FA in grasses and approximately 95% consists of linolenic, linoleic and palmitic acids (Hawke, 1973). Fresh grass contains a high proportion (0.50–0.75) of total FA content as ␣-linolenic acid. Concentrations of ␣-linolenic acid vary with plant, and environmental factors such as stage of maturity, genetic differences (Elgersma et al., 2003a,b), as well as season and light intensity (Dewhurst and King, 1998). Intakes of linolenic acid by cows, fed two cultivars of Lolium perenne with different linolenic acid concentrations (Fig. 1), caused linear increases in milk CLA production (Elgersma et al., 2003a). Quantifying the FA concentrations, and profile, in grasses in response to environmental factors could help in design of management strategies to increase precursors for beneficial FA in ruminant food products. Dewhurst et al. (2003a) concluded that leaf content is very important in determining FA content and that no effect of ploidy was apparent. Some research has been completed to investigate effects of N fertilization on FA concentration in grass. Boufa¨ıed et al. (2003) applied 120 versus 0 kg N/ha on Phleum pratense, which resulted in increases of palmitic (18%), linoleic (12%) and linolenic (40%) acids in the herbage and an overall increase of 26% in the FA concentration. Elgersma et al. (2005) hypothesized that the protein concentration in herbage, the leaf blade proportion of the canopy and the length of the regrowth period of the sward might affect the concentration of fat, and its FA profile in the herbage. Regrowth period affected total FA concentration, and lower concentrations of linolenic and oleic acids occurred after a longer period of regrowth. N application resulted in higher concentrations of all FA, but the FA profile was not affected by N application. However, a longer regrowth period
210
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
Fig. 1. Intake of C18:3 (g/d) of two groups of 6 cows, stall-fed freshly cut perennial ryegrass of cultivars Barlet and Magella, cut daily at a herbage yield of circa 2000 kg DM/ha from June to September, and amount of CLA produced in their milk (g/d), during four sampling dates (Elgersma et al., 2003a).
decreased the proportion of linolenic acid and increased those of linoleic and palmitic acids. A strong positive overall linear relationship occurred between concentrations of total FA and linolenic acid with the N concentration of the herbage. These results were confirmed by further experiments (Witkowska et al., 2006). Lipids in plants are not static entities, but are continuously subject to turnover, meaning that lipid degradation is a normal process in the living plant and that lipases are normally present. Under normal growing conditions this will not have an important influence on the FA composition of the lipid fraction in plants. However, there are at least three times when the lipid fraction in plants, or plant parts, may significantly be modified, being senescence, after detachment (i.e., grazing or cutting) and during storage. In detached plants immediately after cutting, and perhaps during the early stages of ingestion and ensiling, metabolism of plant cells continues and there is still activity of the enzymes in detached and dying tissue. Continuation of processes of respiration and proteolysis are best known, but lipolysis also occurs. In ruminants grazing fresh pastures, the first stages of lipolysis in the rumen could be mediated by plant, rather than microbial, lipases (Lee et al., 2003a,b). Lipases are widely present in living plants and their regulation might be altered due to the double stress of elevated temperature and anoxia imposed on the metabolism of plant cells still intact after ensiling or ingestion by ruminants. Dewhurst and King (1998) studied effects of ensiling on the FA in the resulting silage. Wilting prior to ensiling reduced the content of total FA by almost 30%, with a reduction of up to 40% in linolenic acid. These authors suggested that ensiling has little influence, provided compaction and sealing of the silos is effective, which may not always be the case in ‘big bale’ silages. Adding silage additives, such as formic acid or formalin, substantially reduced losses, which was also noted for formic acid treatment (Doreau and Poncet, 2000). Reducing FA losses due to lipolysis and oxidation during wilting prior to conservation as silage are important strategies to manipulate precursors for CLA in milk.
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
211
Hay making reduced total FA by over 50%, with a higher loss of linolenic acid (Doreau and Poncet, 2000), similar to the loss in haylage (700 g DM/kg) (Elgersma et al., 2003c).
3. Fatty acid conversions in the rumen and mammary gland In contrast to short- and medium-chain FA, ruminants synthesise very little long-chain C18 FA that are desirable in milk. Thus, long-chain FA must be ingested in the feed if they are to be secreted into milk. Between 75% and 90% of linoleic, and 85% and 95% of linolenic, acids are biohydrogenated in the rumen (Kalscheur et al., 1997; Lock and Garnsworthy, 2002; Loor et al., 2004a). In herbage, linolenic acid predominates while maize contains mainly linoleic acid. Commonly used concentrate feed ingredients are often based on plant by-products and are low in fat. Some special ruminant feed products exist in which FA are protected against interference by rumen biohydrogenation (Itabashi and Baevre, 2001). A popular source of vegetable FA in such products is palm oil that is rich in saturated FA. More recently, inclusion in diets of full fat oil seeds high in PUFA has gained popularity. In most oil seeds, linoleic acid predominates as the major PUFA, but linseed contains mainly ␣-linolenic acid. Animal diets could also be supplemented with marine oils, containing predominantely FA of 20 or 22 carbons as the major FA, but this might negatively affect milk flavour, making plant sources, especially forage, the most environmentally sustainable source (Dewhurst et al., 2003a). There are a number of ways to increase the concentration of desired FA in ruminant food products, such as by increasing the amount (i.e., intake) or concentration of their precursors in the diet, by reducing the extent of biohydrogenation in the rumen, and/or by enhancing activity of the 9 —desaturase enzyme that converts vaccenic acid into rumenic acid in the udder. A varying proportion of PUFA, ranging from less than 2%, to over 20%, is recovered in milk as vaccenic acid, an important product of biohydrogenation of both linoleic and linolenic acids. There is a strong relationship between the contents of rumenic and vaccenic acids in cows milk, with the content of vaccenic acid being 2–2.5 times that of rumenic acid. In cows milk, about 70% of rumenic acid originates from conversion of vaccenic acid by 9 —desaturase in the mammary gland and other tissues (Griinari et al., 2000; Bauman et al., 2001). Lipolysis and biohydrogenation have been extensively studied in vitro, notably with soybean oil and, to a lesser extent, with linseed oil. The FA composition of linseed oil resembles that of fresh grass, in that lipids in fresh grass also contain a high proportion of linolenic acid. In experiments of Chow et al. (2004) with linseed oil, an accumulation of the intermediates C18:2 trans-11, cis-15 and vaccenic acid occurred. This was also observed in vivo in the rumen of cows fed linseed oil (Loor et al., 2004b). Because of the similarity in FA profile between fresh grass and linseed oil, the C18:2 trans-11, cis-15 is probably also an important intermediate in the rumen and a precursor for CLA in milk of grass-fed cows. It is likely that this is reflected in the FA profile of milk produced by grass-fed dairy cows. Research in our laboratory showed that, in grazing cows, the C18:2 trans-11 cis-15 content, when expressed as a proportion total FA, ranged between 5 and 8 g/kg FA, whereas on winter diets it never exceeded 1 g/kg FA.
212
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
4. Lipids in milk 4.1. Seasonal effects Milk fat is a mixture of FA, but this overview will focus on proportions of unsaturated fatty acids (UFA), n−3 FA, as well as concentrations of CLA and vaccenic acid, as these are the desired categories of FA in milk fat relative to human health. Seasonal variation in milk FA composition has long been recognized and several authors refer to Riel (1963) in this respect, although it seems to have been first reported by Mattsson (1949) who reported concentrations of conjugated dienoic acids of 6–24 g/kg (with one milk fat with 37 g/kg), and lower levels for stall-fed cows. In The Netherlands, Stadhouders and Mulder (1955) reported a three-fold difference in conjugated dienoic acid concentrations in milk of cows fed in stalls versus pastured (i.e., 7 versus 25 g/kg). Although conjugated dienoic acids include more FA than CLA, these early findings are consistent with recent data. Research in New Zealand (Auldist et al., 1998) and the UK (Lock and Garnsworthy, 2003) revealed seasonal variation in the CLA content of milk fat with highest concentrations, 12.7 and 17.0 g/kg fat, respectively, in grazing cows. Lowest concentrations were in winter and amounted to 6.0 g/kg fat both in New Zealand (Auldist et al., 1998) and the UK (Lock and Garnsworthy, 2003). There was no relationship between milk fat level and CLA proportion of fat. Seasonal fluctuations in milk CLA concentrations were recently measured in The Netherlands (Fig. 2). Nał˛ecz-Tarwacka (Habilitation (PhD Thesis), Warsaw University, Poland) studied 429 cows in 23 farms in central Poland over 2 years. The proportion of UFA was 344 g/kg fat in summer, when all cows were fed fresh grass, and 308 g/kg in winter when they were fed maize silage, grass silage and brewers’ grains. The n−3 FA declined from 9 to 8 g/kg, and the CLA concentration from 7.2 to 5.4 g/kg. In another study, Reklewska et al. (2003) reported CLA concentrations in milk of Black-and-White cows in Poland to be higher in summer (8.4 g/kg) and autumn (8.9 g/kg) versus winter (6.3 g/kg). They also compared
Fig. 2. Seasonal variation for concentration of CLA in Dutch milk (2001–2002) (modified from Ellen et al., 2003).
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
213
Table 1 CLA concentrations (g/kg of milk fat) of cows on different feeding systems in Poland, depending on the season (Reklewska et al., 2003) Feeding system
Summer
Winter
Indoor-pasture ecological Indoor-pasture conventional Indoor TMR
10.0 5.0 6.7
7.1 6.9 5.4
CLA in milk from cows fed a total mixed ration versus pasture and respective values were 6.1 and 11.7 g/kg. A further study compared seasonal changes in cows indoors, on three feeding systems (Table 1, Reklewska et al., 2003). For unknown reasons, and contrary to the general trend of lower CLA concentrations in winter, cows on a conventional indoorpasture system, common in Poland, had a higher value in winter, when no pasture was offered, versus summer when pasture was offered ad libitum. A fast response in CLA content in milk occurred when cows changed from winter feeding to pasture (Kelly et al., 1998), and vice versa (Elgersma et al., 2004a). This was confirmed in further studies where cows were housed and fed only maize silage from October 3, following unrestricted stocking (A. Elgersma, unpublished, Fig. 3). Outcomes were consistent with Chilliard et al. (2001) that the maximum effect is reached within about 5 days. Recent research of Shingfield et al. (2006) suggests that, when feeding fish oil or sunflower oil, this enhancement may not always be consistent, and may even decline with time after an initial increase. We are not aware of such a decline in animals on pasture. 4.2. Regional, farming system and feeding system effects Jensen (2002) and Precht and Molkentin (1995, 2000) have produced extensive reviews on the FA profiles of milk fat. A selection of their data, and others, is in Table 2, although this is not a complete review of available data. Contents of vaccenic acid are also included in Table 2 when available, and some of the data are based upon only 3–5 samples, and others upon more than 1000, notably the data from Germany. Thus, most cases only reflect
Fig. 3. Quick decline in CLA concentrations (g/kg fat) in milk of six cows during a 14-day transition period from grass (unrestricted grazing of perennial ryegrass until 3 October = day 0) to maize silage fed indoors in 2003 (Elgersma, unpublished data).
214
Table 2 CLA, rumenic acid and vaccenic acid contents (mg/g fat) in bulk milk fat Country and season or conditon
Total CLA min
max
mean
max
mean
min
max
1.0 4.9 1.9 1.0 3.6
10.5 18.9 11.9 18.9 13.3
3.5 14.5 8.5 3.5
19.6 44.3 17.3 44.3
4.2
9.3 28.7 17.8 17.2 19.8 9.3 19.2 15.5 8.0
6.0 6.0 7.0 6.6
20.0 44.0 29.0 9.2
4.2
10.3
15.5
9.8
22.5
4.5
3.0
8.2
10.6
7.9
17.0
9.2 7.6 8.7 9.5 7.4
5.2
14.4
5.9 8.2 2.1
9.9 11.1 15.6
3.6
38.1
10.3 8.7 9.4 14.1
6.0 8.5 6.3 5.6
14.0 8.9 16.7 18.2
4.1 9.2 6.4 3.7
2.0 3.0 3.0 2.9
7.0 25.0 12.0 4.5
3.4
2.8
The Netherlands, summer
6.9
4.6
10.9
6.5
The Netherlands, spring/autumn
4.7
3.0
8.5
UK Greece Italy Ireland
Ref.
min
Germany, barn Germany, pasture Germany, transition Germany, all The Netherlands The Netherlands, barn The Netherlands, pasture The Netherlands, transition The Netherlands, winter
Austria Belgium Denmark Spain France
Vaccenic acid
4.5 12.0 7.6 7.5 7.3
14.7 20.0 21.1 17.1 23.6 25.1 19.1 21.0 35.4
Precht and Molkentin (2000) Precht and Molkentin (2000) Precht and Molkentin (2000) Precht and Molkentin (2000) Precht and Molkentin (1995, 2000) Ellen et al. (2001) Ellen et al. (2001) Ellen et al. (2001) G. Ellen, NIZO Food Research, Ede, The Netherlands, personal communication G. Ellen, NIZO Food Research, Ede, The Netherlands, personal communication G. Ellen, NIZO Food Research, Ede, The Netherlands, personal communication Precht and Molkentin (2000) Precht and Molkentin (1995, 2000) Precht and Molkentin (1995, 2000) Precht and Molkentin (1995, 2000) Precht and Molkentin (2000) Precht and Molkentin (1995) Precht and Molkentin (1995, 2000) Precht and Molkentin (1995, 2000) Precht and Molkentin (1995, 2000) Precht and Molkentin (1995, 2000)
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
mean
Rumenic acid
8.7 16.1 23.6
4.6 17.1 4.3
3.4 12.5 3.2
5.5 23.4 7.8
6.7 5.6 8.1 15.0 21.8 11.0 14.0
14.8 7.0 13.0 18.0 7.0 8.0
11.0 18.0 26.0 14.0 22.0
4.5
3.4
6.4
21.1 36.6 51.0
52.8 16.4
18.0 32.0 42.0
42.7 13.1
25.0 42.0 58.0
73.0 26.5
Precht and Molkentin (1995, 2000) Precht and Molkentin (2000) Collomb et al. (2002) Collomb et al. (2002) Collomb et al. (2002) MacGibbon et al. (2001) MacGibbon et al. (2001) Lin et al. (1995) Jensen (2002) ˙ Zegarska and Kuzdzal-Savoie (1988) ˙ Zegarska and Kuzdzal-Savoie (1988)
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
Luxemburg Sweden Switzerland, lowlands Switzerland, mountains Switzerland, highlands New Zealand New Zealand, autumn, milk from 44 herds USA Canada Poland, pasture feeding Poland, indoor feeding
215
216
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
bulk milk from one season, whereas others give a detailed picture of several seasons or circumstances. Data for The Netherlands from Ellen et al. (2001) in Table 2 are raw milk samples from 18 dairy farms taken four times over a year in the four seasons. Data from G. Ellen, NIZO Food Research, Ede, The Netherlands, personal communication in Table 2 are samples from tankers of raw milk from the whole country once a month over 12 months. This difference in study design might explain the smaller variation in FA concentrations in the second study. Average concentrations of rumenic acid in bulk milk in most countries are 4–10 g/kg of fat (Table 2), and concentrations during pasture feeding are 2–3 times those during barn feeding. The highest concentrations of rumenic acid are in milk fat from Ireland, New Zealand and Switzerland, which probably relates to long periods of pasture feeding and, for Switzerland, to unique meadow grasses and herbs from the mountains and highlands. Data for milk from the Swiss mountains are consistent with rumenic acid concentrations in Italian cheese, produced from milk of cows grazing mountain pastures, a median rumenic acid content of 16.7 g/kg fat, compared with 7.1 g/kg fat in cheese from barn-fed cows (Innocente et al., 2002). Data in Table 2 also shows that there is a strong positive relationship between concentrations of rumenic and vaccenic acids in milk fat, with vaccenic acid concentrations being 2–2.5 times those of rumenic acid. Collomb et al. (2002) found large differences in milk FA patterns related to the altitude of mountain pastures. The lowland cows were fed maize and concentrate in the barn, as well as having access to pasture, whereas cows in the mountains (900–1210 m) and highland sites (1275–2120 m) were only on pasture. The increase in PUFA in milk fats from the lowland to the highland cows was mainly due to the increase in rumenic acid. Jahreis et al. (1997) compared conventional farming with high external inputs of fertiliser and concentrates, with or without grazing during summer, with low exernal input ecological farming with summer grazing. It was observed that organically produced milk had the highest contents of both CLA and vaccenic acids in its milk fat, especially during the May to September grazing period. The authors explained the differences by the different feeding strategies between the systems, and claimed that the ‘green’ feeds in organic farming were richer in PUFA than the silages and concentrates fed in conventional farming, that the grass/legume silages were richer in PUFA compared to maize silages, and indicated that rations higher in fibre cause specific rumen bacterial populations, as measured by a higher content of branched-chain FA in milk fat. In another comparison (Dewhurst, 2003c) bulk milk samples were obtained from 10 organic, and 8 conventional, dairy farms during winter. The most notable difference between the herd types was in annual milk production, reflecting very different levels of concentrate feeding. A covariance analysis showed that many of the differences in FA composition between organic and conventional milk were related to milk production level of the cows. However, after accounted for effects of milk yield, some effects of organic farming remained, which were probably the result of the different range of dietary ingredients used by organic farmers. It is not clear whether the higher concentrations of palmitic acid, and lower concentrations of stearic acid, in organic milk were a result of differences in dietary fat sources or effects of rumen fermentation patterns on de novo synthesis of FA (Dewhurst, 2003c). The higher concentration of linolenic acid in organic milk is consistent with recent observations of higher concentrations of this FA in milk produced from red or white clover
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
217
Fig. 4. Changes in the concentrations (g/kg fat) of rumenic, vaccenic and linolenic acids and saturated, monoand poly-unsaturated fatty acids (SFA, MUFA, PUFA) in milk of six cows that were stall-fed freshly cut perennial ryegrass from June to September, and after 1 month unrestricted stocking on a pasture with a more diverse botanic composition, from September to October (Elgersma et al., 2003d).
silages compared to milk produced from grass silage (Dewhurst et al., 2003b). With a low level of concentrate feeding, and red clover silage as sole forage, these authors showed concentrations of linolenic acid in milk to be three-fold those of the concentrations in milk from cows fed grass silage (Dewhurst et al., 2003b). In addition to the difference between fresh and conserved forage, there also seems to be an effect of grazing per se. The CLA content of milk from stall-fed cows on cut grass was lower than that in milk from cows that grazed grass, as occurred in an indirect comparison (Fig. 4) by Elgersma et al. (2003d). Indeed, cows on pasture (Dhiman et al., 1999a; Elgersma et al., 2004a) grazing lush fresh grass (Dewhurst et al., 2003a; Elgersma et al., 2003d; Khanal and Olson, 2004) at a high herbage allowance (Elgersma et al., 2004b; Fig. 5), produced milk with the highest concentrations of PUFA. A review of the effect of pasturing on the CLA content of milk is in Table 3 . 4.3. Animal and breed effects ˙ Zegarska et al. (2001) reported milk FA profiles in summer milk from pastured cows and found higher CLA concentrations for Polish red (11.9 g/kg) versus Black-and-White
218
Table 3 Polyunsaturated FA and CLA in milk of cows on pasture Treatment
Cows
DIMa
Code
Treatment
Milk (kg/d)
Fat (g/kg)
0 0
Control
10 5.0
101 48.0
Average
Control diets indoors STDEV
33.4 5.9
35.5 3.3
Jahreis et al. (1997)
1 2 3
350 1600 260
Year round Year round Year round
Pasture Indoor Ecological
Kelly et al. (1998) Lawless et al. (1998)
4 5
8 16
May Control
Pasture US Pasture + 3 kg concentrates
29.6 20.1
37.2 38.9
10.9 16.6
22.5 23.3
9.5 7.1
Dhiman et al. (1999a)
6 7 8
12 11 12
September September September
1/3 Pasture 2/3 Pasture All Pasture
24.5 17.5 14.5
35.1 36.4 33.7
8.9 14.3 22.1
42.7 27.1 14.0
8.1 14.6 20.2
Auldist et al. (1998)
9 10 11
17 18 13
43 118 220
Early Mid Late
Spring pasture NZ Spring pasture NZ Spring pasture NZ
18.5 14.3 11.7
42.2 45.3 46.3
9.7 11.1 12.7
12
10
133
June
27.5
32.3
7.2
18.2
7.1
0.078
13
10
133
June
Pasture Holsteins, C4 grass Pasture Jerseys, C4 grass
24.8
36.8
5.9
18.6
7.5
0.071
14 15 16 17 18
965 965 965 965 965
46.2 46.2 44.8 48.3 50.8
10.8 9.6 10.0 9.0 12.7
White et al. (2001)
Thomson and Van der Poel (2000)
59
November December January February March
Pasture NZ Pasture NZ Pasture NZ Pasture NZ Pasture NZ
CLA (g/kg FA) 4.4 1.1
C18:2 (g/kg FA) 27.0 5.7
C18:3 (g/kg FA) 4.7 2.0
6.1 3.4 8.0
t11-C18:1 (g/kg FA)
C14:1/C14
14.3 6.6
0.102 0.056
22.1 12.1 26.7 0.093 0.118
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
Experiment
6 6 6 6 6 6 6
June July July July/August August August Sept
Pasture NL, period 1 Pasture NL, period 2 Pasture NL, period 3 Pasture NL, period 4 Pasture NL, period 5 Pasture NL, period 6 Pasture NL, period 7
30.0 29.2 30.3 29.3 26.7 23.6 23.7
40.0 39.0 39.0 38.0 41.0 41.0 42.0
10.2 12.0 14.3 15.7 16.9 14.5 15.2
21.6 24.0 20.4 17.7 19.9 19.0 16.8
7.9 7.0 9.6 6.0 6.3 5.5 6.3
29.9 31.0 34.4 37.1 37.3 32.3 32.8
Elgersma et al. (2004a)
26
6
October
Pasture NL
19.7
43.7
24.3
10.4
8.9
46.2
Lock and Garnsworthy (2003)
27 28 29 30 31
45 45 45 45 45
May June July August Sept
Pasture UK Pasture UK Pasture UK Pasture UK Pasture UK
27.0 29.0 25.0 27.0 30.0
42.0 37.0 39.0 36.0 34.0
14.0 17.0 14.0 9.0 10.0
22.0 28.0 38.0 36.0 36.0
8.0 10.0 10.0 11.0 12.0
45.0 40.0 26.0 35.0 36.0
a DIM = Days in milk.
186 180 227 186 186
0.079 0.073 0.064 0.059 0.056
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
Elgersma et al. (2003a)
19 20 21 22 23 24 25
219
220
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
Fig. 5. Concentration of CLA (g/kg fat) in milk of two groups of six cows each with continuous stocking on perennial ryegrass pastures, after a week with a high herbage allowance (44 kg DM/d) (day 0), and 3.5 and 7 days after reducing the herbage allowance to 22 kg DM/d (Elgersma et al., 2004b).
(9.4 g/kg). Other authors (White et al., 2001; Kelsey et al., 2003) noted small, but significant, breed differences. Individual animal variation may also be important as cows fed the same diet had a threefold difference in milk conjugated linoleic acid (CLA) content (Kelsey et al., 2003). These authors found that breed (i.e., Holstein versus Brown Swiss), parity and lactation stage had little relationship to individual variation in milk fat content of CLA, and the CLA-desaturase index, and concluded that these CLA variables were essentially independent of milk yield, milk fat proportion and milk fat yield. Elgersma et al. (2004a) reported a range in CLA concentrations in milk of six grass grazed cows, of 14–36 g/kg of milk fat and 4.0–5.8 g/kg, at the end of a 2 weeks transition period to a 1:1 grass/maize silage diet. In a second experiment, the CLA contents in milk fat of 12 cows ranged from 12.4 to 27.8 g/kg on grazed grass, and from 4.0 to 8.6 g/kg 4 days after transition to maize silage. In general, CLA concentrations differed among cows, but patterns in response to diet changes were similar. The ranking of cows for the CLA content in their milk at the various sampling days was similar (Elgersma et al., 2004a), consistent with Lock and Garnsworthy (2003) who also found consistency in the ranking of individual cows in cis-9, trans-11 C18:2 content in milk fat with increased time on the same diet, or when cows changed diets. Provided the trait is at least moderately heritable, this could offer scope for selecting high CLA milk cows for breeding.
5. Trends and future perspectives During the last few decades, the FA composition of milk has become less favorable in The Netherlands as essential FA and CLA concentrations have declined. In the 1960s, summer Dutch farm milk contained, on average, 15 g/kg CLA (Elgersma, unpublished results), but
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
221
Fig. 6. Relationship between concentrations of CLA (g/kg fat) and unsaturated fatty acids (UFA) in milk of individual cows in two experiments with A. 6 cows (2000) and B. 12 cows (2002) during transition from unrestricted grazing to indoor feeding with silage (based on data from Elgersma et al., 2004a).
in 2001–2002 (Fig. 2) the average was 7 g/kg between June and August, and 5 g/kg in spring and autumn (Ellen et al., 2003). With low-fat dairy products being marketed, human intake of CLA is declining even further as ruminant food products are the main source of human CLA intake. Health effects of CLA need further study in humans, but the beneficial effect of unsaturated FA in general now seems commonly accepted. As CLA concentrations are correlated with those of unsaturated FA, they could perhaps be used as indicators of the FA composition milk (Fig. 6). The potential of plant breeding and management to increase the beneficial FA content of grass and clover species was recently reviewed by Dewhurst et al. (2003a). As fertilization and herbage allowance can be easily managed by farmers, it might be a feasible way to obtain higher concentrations of FA in herbage. As well, the timing of cutting or grazing (i.e., the regrowth stage at which herbage is harvested), can influence herbage quality.
222
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
The issues discussed in this review regarding the benefits of fresh herbage, and in particular grazing, could perhaps reverse the currently increasing trend for cows in The Netherlands to be kept indoors year round. However, effects on milk production, landscape values, animal welfare and public opinion will also play a role in the debate. Some economic analyses show benefits of grazing, depending on the farm size and spatial situation, as conserved feed is more expensive than fresh herbage (Van den Pol-van Dasselaar, 2005). However, cows with very high milk yield potential cannot meet their energy requirements from grass alone, partly due to insufficient intake (Taweel et al., 2005). Scollan et al. (2005) stated that grassland offers considerable scope to help create product differentiation in increasingly competitive markets. Farmers from a small Dutch dairy cooperative that produce milk from grazed grass now receive a premium payment in addition to the base milk price. A yoghurt producer buys milk from grazing dairies, pays the farmers a premium, and mentions the milk source in the product information for the consumer. In these cases, primary producers benefit from the higher market value at the end of the production chain. 6. Conclusions The FA profile of milk fat can be modified by feeding strategies, and there may be longer-term options by animal breeding. There are possibilities for a chain-approach from farm to processor to consumer, some examples were presented, and such an integrated approach is essential if scientific findings are to be put into practice. However, there remain questions about human health claims of various milk FA’s. Research, and standard protocols, for sampling, storage and FA analysis in forages are needed, and there is current research underway in this area in many parts of the world. References Aro, A., Mannisto, S., Salminen, I., Ovaskainen, M.L., Kataja, V., Uusitupa, M., 2000. Inverse association between dietary and serum conjugated linoleic acid and risk of breast cancer in post-menopausal women. Nutr. Cancer 38, 151–157. Ascherio, A., Rimm, E.B., Giovannucci, E.L., Spiegelman, D., Stampfer, M., Willett, W.C., 1996. Dietary fat and risk of coronary heart disease in men: cohort follow up study in the United States. Brit. Med. J. 313, 84–90. Auldist, M.J., Walsh, B.J., Thomson, N.A., 1998. Seasonal and lactational influences on bovine milk composition in New Zealand. J. Dairy Res. 65, 401–411. Banni, S., Angioni, E., Murru, E., Carta, G., Melis, M.P., Bauman, D., Dong, Y., Ip, C., 2001. TVA acid feeding increases tissue levels of conjugated linoleic acid and suppresses development of premalignant lesions in rat mammary gland. Nutr. Cancer 41, 91–97. Bauchart, D., V´erit´e, R., R´emond, B., 1984. Long-chain fatty acid digestion in lactating cows fed fresh grass from spring to autumn. Can. J. Anim. Sci. 64 (Suppl.), 330–331. Bauman, D.E., Corl, B.A., Baumgard, L.H., Griinari, J.M., 2001. Conjugated linoleic acid (CLA) and the dairy cow. In: Garnsworthy, P.C., Wiseman, J. (Eds.), Recent Advances in Animal Nutrition 2001. Nottingham University Press, Nottingham, UK, pp. 221–250. Belury, M.A., 2002. Dietary conjugated linoleic acid in health: physiological effects and mechanisms of action. Annu. Rev. Nutr. 22, 505–531. Boufa¨ıed, H., Chouinard, P.Y., Tremblay, G.F., Petit, H.V., Michaud, R., B´elanger, G., 2003. Fatty acids in forages. I. Factors affecting concentrations. Can. J. Anim. Sci. 83, 501–511.
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
223
Chilliard, Y., Ferlay, A., Doreau, M., 2001. Effect of different types of forages, animal fat or marine oils in cow’s diet on milk fat secretion and composition, especially conjugated linoleic acid (CLA) and polyunsaturated fatty acids. Livest. Prod. Sci. 70, 31–48. Chow, T.T., Fievez, V., Moloney, A.P., Raes, K., Demeyer, D., DeSmet, S., 2004. Effect of fish oil on in vitro rumen lipolysis, apparent biohydrogenation of linoleic and linolenic acid and accumulation of biohydrogenation intermediates. Anim. Feed Sci. Tech. 117, 1–12. Collomb, M., B¨utikofer, U., Sieber, R., Jeangros, B., Bosset, J.-O., 2002. Composition of fatty acids in cow’s milk fat produced in the lowlands, mountains and highlands of Switzerland using high-resolution gas chromatography. Int. Dairy J. 12, 649–659. Corl, B.A., Barbano, D.M., Bauman, D.E., Ip, C., 2003. Cis-9 trans-11 CLA derived endogenously from trans-11 18:1 reduces cancer risk in rats. J. Nutr. 133, 2893–2900. Dewhurst, R.J., King, P.J., 1998. Effects of extended wilting, shading and chemical additives on the fatty acids in laboratory grass silages. Grass Forage Sci. 53, 219–224. Dewhurst, R.J., Scollan, N.D., Lee, M.R.F., Ougham, H.J., Humphreys, M.O., 2003a. Forage breeding and management to increase the beneficial fatty acid content of ruminant products. Proc. Nutr. Soc. 62, 329–336. Dewhurst, R.J., Fisher, W.J., Tweed, J.K.S., Wilkins, R.J., 2003b. Comparison of grass and legume silages for milk production. 1. Production responses with different levels of concentrate. J. Dairy Sci. 86, 2598–2611. Dewhurst, R.J., 2003c. Fatty Acids in Milk Fat from Organic Dairy Farms. Elm Farm Research Centre Bulletin. Elm Farm Research Centre, Hamstead Marshall, Newbury, Berks, UK, p. 11. Dhiman, T.R., Anand, G.R., Satter, D., Pariza, M.W., 1999a. Conjugated linoleic acid content of milk from cows fed different diets. J. Dairy Sci. 82, 2146–2156. Dhiman, T.R., Helmink, D., McMahon, D.J., Fife, R.L., Pariza, M.W., 1999b. Conjugated linoleic acid content of milk and cheese from cows fed extruded oilseeds. J. Dairy Sci. 82, 412–419. Doreau, M., Poncet, C., 2000. Ruminal biohydrogenation of fatty acids originating from fresh or preserved grass. Repr. Nutr. Dev. 40, 201. Elgersma, A., Ellen, G., Dekker, P.R., van der Horst, H., Boer, H., Tamminga, S., 2003a. Effects of perennial ryegrass (Lolium perenne) cultivars with different linolenic acid contents on milk fatty acid composition. Asp. Appl. Biol. 70, 107–114. Elgersma, A., Ellen, G., van der Horst, H., Muuse, B.G., Boer, H., Tamminga, S., 2003b. Influence of cultivar and cutting date on the fatty acid composition of perennial ryegrass. Grass Forage Sci. 58, 323–331 (also Erratum Grass Forage Sci. 59, 104). Elgersma, A., Ellen, G., van der Horst, H., Muuse, B.G., Boer, H., Tamminga, S., 2003c. Comparison of the fatty acid composition of fresh and ensiled perennial ryegrass (Lolium perenne L.), affected by cultivar and regrowth interval. Anim. Feed Sci. Tech. 108, 191–205. Elgersma, A., Tamminga, S., Ellen, G., 2003d. Comparison of the effects of grazing and zero-grazing of grass on milk fatty acid composition of dairy cows. Grassl. Sci. Eur. 8, 271–274. Elgersma, A., Ellen, G., van der Horst, H., Muuse, B.G., Boer, H., Tamminga, S., 2004a. Quick changes in milk fat composition after transition from fresh grass to a silage diet and effects on consumer health benefits. Anim. Feed Sci. Tech. 117, 13–27. Elgersma, A., Ellen, G., Tamminga, S., 2004b. Rapid decline of contents of beneficial omega-7 fatty acids in milk from grazing cows with decreasing herbage allowance. Grassl. Sci. Eur. 9, 1136–1138. Elgersma, A., Maudet, P., Witkowska, I.M., Wever, A.C., 2005. Effects of N fertilization and regrowth period on fatty acid concentrations in perennial ryegrass (Lolium perenne L.). Ann. Appl. Biol. 147, 145–152. Ellen, G., te Giffel, M., Slaghuis, B., 2001. Invloed van melkveevoeding op de vetzuursamenstelling van melk. Zuivelzicht 93, 26–27. Ellen, G., te Giffel, M., Sprong, M., 2003. Be¨ınvloeding vetzuursamenstelling van melk via voer. Voedingsmagazine 16, 12–17. Griinari, J.M., Corl, B.A., Lacy, S.H., Chouinard, P.Y., Nurmela, K.V.V., Bauman, D.E., 2000. Conjugated linoleic acid is synthesized endogenously in lactating dairy cows by 9 desaturase. J. Nutr. 130, 2285–2291. Grundy, S.M., Vega, G.L., 1998. Plasma cholesterol responsiveness to saturated fatty acids. Am. J. Clin. Nutr. 47, 822–824. Havel, R.J., 1997. Milk fat consumption and human health: recent NIH and other American governmental recommendations. In: Welch, R.A.S., Burns, D.J.W., Davis, S.R., Popay, A.I., Prosser, C.G. (Eds.), Milk Composition, Production And Biotechnology. CAB International, Wallingford, UK, pp. 13–22.
224
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
Hawke, J.C., 1973. Lipids. In: Butler, G.W., Bailey, R.W. (Eds.), Chemistry and Biochemistry of Herbage. Academic Press, London, UK, pp. 213–263. Innocente, N., Praturlon, D., Corradini, C., 2002. Fatty acid profile of cheese produced with milk from cows grazing on mountain pastures. Ital. J. Food Sci. 14, 217–224. Ip, C., Banni, E., Carta Angioni, G., McGinley, J., Thompson, H.J., Barbano, D., Bauman, D., 1999. Conjugated linoleic acid-enriched butter fat alters mammary gland morphogenesis and reduces cancer risk in rats. J. Nutr. 129, 2135–2142. Itabashi, H., Baevre, L., 2001. Trends in milk composition: results of a survey by IDF. Bull. Int. Dairy Fed. 366, 9–14. Jahreis, G., Fritsche, J., Steinhart, H., 1997. Conjugated linoleic acid in milk fat: high variation depending on production system. Nutr. Res. 17, 1479–1484. Jensen, R.G., 2000. Invited review: the composition of bovine milk lipids. J. Dairy Sci. 85, 295–350. Kalscheur, K.F., Teter, B.B., Piperova, L.S., Erdman, R.A., 1997. Effect of dietary forage concentration and buffer addition on duodenal flow of trans-C18:1 fatty acids and milk fat production in dairy cows. J. Dairy Sci. 80, 2104–2114. Kelly, M.L., Kolver, E.S., Bauman, D.E., Amburgh, M.E., van, Muller, L.D., 1998. Effect of intake of pasture on concentrations of conjugated linoleic acid in milk of lactating cows. J. Dairy Sci. 81, 1630–1636. Kelsey, J.A., Corl, B.A., Collier, R.J., Bauman, D.E., 2003. The effect of breed, parity, and stage of lactation on conjugated linoleic acid (CLA) in milk fat from dairy cows. J. Dairy Sci. 86, 2588–2597. Kennelly, J.J., 2001. The fatty acid composition of milk fat as influenced by feeding oilseeds. Bull. Int. Dairy Fed. 366, 28–36. Khanal, R.C., Olson, K.C., 2004. Factors affecting conjugated linolenic acid (CLA) content in milk, meat, and egg: a review. Pakistan J. Nutr. 3, 82–98. Lavillonni`ere, F., Martin, J.C., Bougnoux, P., S´eb´edio, J.-L., 1998. Analysis of conjugated linoleic acid isomers and content in French cheeses. J. Am. Oil Chem. Soc. 75, 343–352. Lawless, F., Murphy, J.J., Harrington, D., Devery, R., Stanton, C., 1998. Elevation in conjugated cis-9, trans-11 octadecadienoic acid in bovine milk because of dietary supplementation. J. Dairy Sci. 81, 3259–3267. Lee, M.R.F., Harris, L.J., Dewhurst, R.J., Merry, R.J., Scollan, N.D., 2003a. The effect of clover silages on long-chain fatty acid rumen transformations and digestion in beef steers. Anim. Sci. 76, 491–501. Lee, M.R.F., Winters, A.L., Scollan, N.D., Dewhurst, R.J., Theodorou, M.K., Minchen, F.R., 2003b. Plant-mediated lypolysis and proteolysis in red clover with different polyphenol exidase activities. J. Sci. Food Agric. 84, 1639–1645. Lin, H., Boylston, T.D., Chang, M.J., Luedecke, L.O., Shultz, T.D., 1995. Survey of the conjugated linoleic acid contents of dairy products. J. Dairy Sci. 78, 2358–2365. Lock, A.L., Garnsworthy, P.C., 2002. Independent effects of dietary linoleic and linolenic fatty acids on the conjugated linoleic acid content of cow’s milk. Anim. Sci. 74, 163–176. Lock, A.L., Garnsworthy, P.C., 2003. Seasonal variation in milk conjugated linoleic acid and Δ9 —desaturase activity in dairy cows. Livest. Prod. Sci. 79, 47–59. Lock, A.L., Corl, B.A., Barbano, D.M., Bauman, D.E., Ip, C., 2004. The anticarcinogenic effect of trans-11 18:1 is dependent on its conversion to cis-9, trans-11 CLA by Δ9 —desaturase in rats. J. Nutr. 134, 2698– 2704. Loor, J.J., Ueda, K., Ferlay, A., Chilliard, Y., Doreau, M., 2004a. Biohydrogenation, duodenal flow, and intestinal digestibility of trans fatty acids and conjugated linoleic acids in response to dietary forage:concentrate ratio and linseed oil in dairy cows. J. Dairy Sci. 87, 2472–2485. Loor, J.J., Ueda, K., Ferlay, A., Chilliard, Y., Doreau, M., 2004b. Diurnal profiles of conjugated linoleic acids and trans fatty acids in ruminal fluid from cows fed a high concentrate diet supplemented with fish oil, linseed oil, or sunflower oil. J. Dairy Sci. 87, 2468–2471. MacGibbon, A.K.H., Van der Does, Y.E.H., Fong, B.Y., Robinson, N.P., Thomson, N.A., 2001. Variations in the CLA content of New Zealand milkfat. Aust. J. Dairy Technol. 56, 158. Mattsson, S., 1949. Poly-unsaturated fatty acids in butter and their influence on the oxidation of butter. Methods of analysis and preliminary results. In: Proceedings of the XIIth International Dairy Congress, Stockholm, pp. 308–324, Section II. Nał˛ecz-Tarwacka, T. Effect of selected factors on the functional component of milk fat in dairy cows. Habilitation (PhD Thesis), Warsaw University, Poland, Submitted for publication.
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
225
Precht, D., Molkentin, J., 1995. Trans fatty acids: implications for health, analytical methods, incidence in edible fats and intake. Die Nahrung 39, 343–374. Precht, D., Molkentin, J., 2000. Frequency distributions of conjugated linoleic acid and trans fatty acid contents in European bovine milk fats. Michwissenschaft 55, 687–691. Reklewska, B., Bernatowicz, E., Reklewski, Z., Nał˛ecz-Tarwacka, T., Kuczy´nska, B., Zdziarski, K., Oprz˛adek, A., 2003. Concentration of milk functional components in Black-and-White cows, depending on the season and feeding system (in Polish). Zeszyty Naukowe Przegl˛adu Hodowlanego 68, 85–98. Riel, R.R., 1963. Physico-chemical characteristics of Canadian milk fat. Unsaturated fatty acids. J. Dairy Sci. 46, 102–106. Salminen, I., Mutanen, M., Jauhiainen, M., Aro, A., 1998. Dietary trans fatty acids increases conjugated linoleic acid levels in human serum. Nutr. Biochem. 9, 93–98. Santora, J.E., Palmquist, D.L., Roehrig, K.L., 2000. Trans-vaccenic acid is desaturated to conjugated linoleic acid in mice. J. Nutr. 130, 208–215. Scollan, N.D., Dewhurst, R.J., Moloney, A.P., Murphy, J.J., 2005. Improving the quality of products from grassland. In: McGilloway, D.A. (Ed.), Grassland: a global resource. Wageningen Academic Publishers, Wageningen, The Netherlands, pp. 41–56. Shingfield, K.J., Reynolds, C.K., Hervas, G., Griinari, J.M., Grandison, A.S., Beever, D.E., 2006. Examination of the persistency of milk fatty acid composition responses to fish oil and sunflower oil in the diet of dairy cows. J. Dairy Sci. 89, 714–732. Stadhouders, J., Mulder, H., 1955. The composition of Dutch butterfat. 1. Seasonal variations in the unsaturated fatty acid composition of butter fat. Neth. Milk Dairy J. 9, 182–193. Tamminga, S., 2001. Effects of feeds, feed composition and feed strategy on fat content and fatty acid composition in milk. Bull. Int. Dairy Fed. 366, 15–24. Taweel, H.Z., Tas, B.M., Smit, H.J., Elgersma, A., Dijkstra, J., Tamminga, S., 2005. Effects of feeding perennial ryegrass with an elevated concentration of water-soluble carbohydrates on intake, rumen function and performance of dairy cows. Anim. Feed Sci. Technol. 121, 243–256. Thomson, N.A., Van der Poel, W., 2000. Seasonal variation of the fatty acid composition of milk fat from Friesian cows grazing pasture. Proc. NZ Soc. Anim. Prod. 60, 314–317. Turpeinen, A.M., Mutanen, M., Aro, A., Salminen, I., Basu, S., Palmquist, D.L., Griinari, J.M., 2002. Bioconversion of vaccenic acid to conjugated linoleic acid in humans. Am. J. Clin. Nutr. 76, 504–510. Van den Pol-van Dasselaar, A., 2005. Grazing in transition (in Dutch). Animal Sciences Group, Lelystad, The Netherlands. PraktijkRapport Rundvee 81, 127. White, S.L., Bertrand, J.A., Wade, M.R., Washburn, S.P., Green Jr., J.T., Jenkins, T.C., 2001. Comparison of fatty acid content of milk from Jersey and Holstein cows consuming pasture or a total mixed ration. J. Dairy Sci. 84, 2295–2301. Williams, C.M., 2000. Dietary fatty acids and human health. Ann. Zootech. 49, 165–180. Witkowska, I.C., Wever A.C., Elgersma A., 2006. Seasonal effects on fatty acid concentrations in perennial ryegrass (Lolium perenne L.) in relation to nitrogen and regrowth interval. Eur. J. Agron, Submitted for publication. ˙ Zegarska, A., Jaworski, J., Paszczyk, B., Charkiewicz, J., Borejszo, Z., 2001. Fatty acid composition with emphasis on trans C18:1 isomers of milk fat from lowland Black-and-White and Polish Red cows. Pol. J. Food Nutr. Sci. 4, 41–44. ˙ Zegarska, Z., Kuzdzal-Savoie, 1988. Seasonal effects on the fatty acids content in milk fat. Michwissenschaft 43, 777–779.
Review
Modifying milk composition through forage A. Elgersma a,∗ , S. Tamminga b , G. Ellen c a
Wageningen University, Crop and Weed Ecology Group, Graduate School of Production Ecology and Resource Conservation (PE&RC), Haarweg 333, 6709 RZ Wageningen, The Netherlands b Wageningen University, Animal Sciences Group, Graduate School Wageningen Institute for Animal Sciences (WIAS), Marijkeweg 40, 6709 PG Wageningen, The Netherlands c NIZO Food Research, P.O. Box 20, 6710 BA Ede, The Netherlands Accepted 16 June 2006
Abstract The fatty acid (FA) composition of cows milk has become less favorable to human health in the last four decades due to changed feeding and management practices, notably higher proportions of concentrates and silages in diets with less grazing. Essential FA and conjugated linoleic acid (CLA) concentrations have generally declined and, with more ‘low-fat’ dairy products, human intake of these FA has declined even further since ruminant food products are the main source of human CLA intake. Changing societal drivers and consumer demands require dairy production systems that provide food products through sustainable production systems. Milk FA were examined in milk produced in different regions of the world, in the different seasons of the year, and under different feeding systems. FA levels were examined in forages, concentrates and milk. Milk from cows fed fresh green forage, especially those grazing grass, had a much higher unsaturated:saturated FA proportion, with more polyunsaturated FA and more CLA (in particular C18:2 cis-9, trans-11), than milk from silage-fed cows. Farmers from some dairy cooperatives in The Netherlands that produce milk from grazed grass now receive a premium payment in addition to the base milk price, so that primary producers can benefit from the higher market value at the end of the production chain. © 2006 Elsevier B.V. All rights reserved. Keywords: Forage; Silage; Feeding system; Seasonal change; Milk fatty acids
Abbreviations: CLA, conjugated linoleic acid; DM, dry matter; FA, fatty acids; LDL, low density lipoprotein; MUFA, monounsaturated FA; PUFA, polyunsaturated FA; UFA, unsaturated FA ∗ Corresponding author. Tel.: +31 317 483523; fax: +31 317 485572. E-mail address: [email protected] (A. Elgersma). 0377-8401/$ – see front matter © 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.anifeedsci.2006.06.012
208
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
Contents 1. 2. 3. 4.
5. 6.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Lipids in plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Fatty acid conversions in the rumen and mammary gland . . . . . . . . . . . . . . . . . . . . . . . . . . . Lipids in milk . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Seasonal effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Regional, farming system and feeding system effects . . . . . . . . . . . . . . . . . . . . . . . . 4.3. Animal and breed effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Trends and future perspectives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
208 209 211 212 212 213 217 220 222 222
1. Introduction Changing societal drivers (e.g., landscape values, animal welfare) and consumer demands (e.g., tasty/healthy products) require systems that provide desired human foods produced through sustainable production processes. High-fat humen diets, especially those rich in saturated fats, are often claimed to have detrimental effects on cardiovascular disease risk factors such as blood low density lipoprotein (LDL) cholesterol (Ascherio et al., 1996; Williams, 2000). Dairy products contribute 15–20% of human intake of total fat, 25–33% of saturated fat and about 15% of dietary cholesterol in the USA (Havel, 1997). At present, about 2% of total fatty acids (FA) in milk are polyunsaturated (PUFA) and about 70% are saturated, but less than 40% of saturated FA are in categories considered to be less healthy. These values can be modified by changing the animal diets (Tamminga, 2001; Kennelly, 2001; Chilliard et al., 2001), and it is thought that lauric acid (C12:0), but especially myristic (C14:0) and palmitic (C16:0) acid, raise total and LDL cholesterol, whereas stearic acid (C18:0) is neutral relative to the monounsaturated fatty acid (MUFA) oleic acid (C18:1) in animal fats (Grundy and Vega, 1998). Cardiovascular risk might be reduced by lowering intake of undesirable saturated FA and/or by making alterations in the FA profile of the fat consumed. Increasing the concentration of desired FA in ruminant products is receiving current attention. The main n−3 FA in milk is ␣-linolenic acid (C18:3 cis-9, cis-12, cis-15), and another category of PUFA is conjugated linoleic acid (CLA), the main isomer in milk being rumenic acid (C18:2 cis-9, trans-11). The MUFA in milk consist mainly of C18:1 cis-9 (oleic acid) and also C18:1 trans-11 (vaccenic acid). Rumenic and vaccenic acids are both trans-11 FA produced by rumen microorganisms and are unique to ruminant fats. Rumenic acid has been associated with anticarcenogenic properties in rats (Corl et al., 2003; Ip et al., 1999) and possibly in humans (Aro et al., 2000; Belury, 2002). Other potential beneficial effects of CLA for human health were mentioned, but more work is needed to elucidate the safety and efficacy of isomers and their required doses (Belury, 2002). Ingested vaccenic acid can be converted into rumenic acid in mammals, including humans (Salminen et al., 1998; Santora et al., 2000). Turpeinen et al. (2002) estimated that, on average, humans endogenously convert 19% of dietary vaccenic acid into rumenic acid. Banni et al. (2001)
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
209
demonstrated that feeding vaccenic acid to rats, at 2% of the diet, not only increased tissue concentrations of rumenic acid, but also had a protective effect against development of mammary tumours, a similar effect to that later reported by Lock et al. (2004). This implies that, when calculating the dietary intake of rumenic acid, it is reasonable to add 20% of the vaccenic acid in the diet. The CLA contents in dairy product fats are comparable to those of the milk fat from which these products are obtained (Lavillonni`ere et al., 1998; Dhiman et al., 1999b). As milk FA composition is mainly determined by feed composition (i.e., the FA composition of the feed (Khanal and Olson, 2004), and feeding strategy (Tamminga, 2001)), effects of forage, feed and feeding systems will be discussed.
2. Lipids in plants Dairy cow diets are usually composed of a mix of fresh forages, mainly leaf blades, conserved forages (i.e., herbage leaf blades and also stems in spring; seeds and stems in case of forage maize) and concentrates (i.e., plant seeds). Diet composition of dairy cattle differs greatly among seasons and regions of the world. Some information is available about the lipid concentration, and its FA profile, of forages and the factors influencing them. The lipid fraction in leaves of herbs and grasses ranges from 30 to 100 g/kg DM, much of which is contributed by chloroplast lipids (Bauchart et al., 1984). Sources of variation in lipid concentration are plant species, growth stage, temperature and light intensity (Hawke, 1973), but there are five major FA in grasses and approximately 95% consists of linolenic, linoleic and palmitic acids (Hawke, 1973). Fresh grass contains a high proportion (0.50–0.75) of total FA content as ␣-linolenic acid. Concentrations of ␣-linolenic acid vary with plant, and environmental factors such as stage of maturity, genetic differences (Elgersma et al., 2003a,b), as well as season and light intensity (Dewhurst and King, 1998). Intakes of linolenic acid by cows, fed two cultivars of Lolium perenne with different linolenic acid concentrations (Fig. 1), caused linear increases in milk CLA production (Elgersma et al., 2003a). Quantifying the FA concentrations, and profile, in grasses in response to environmental factors could help in design of management strategies to increase precursors for beneficial FA in ruminant food products. Dewhurst et al. (2003a) concluded that leaf content is very important in determining FA content and that no effect of ploidy was apparent. Some research has been completed to investigate effects of N fertilization on FA concentration in grass. Boufa¨ıed et al. (2003) applied 120 versus 0 kg N/ha on Phleum pratense, which resulted in increases of palmitic (18%), linoleic (12%) and linolenic (40%) acids in the herbage and an overall increase of 26% in the FA concentration. Elgersma et al. (2005) hypothesized that the protein concentration in herbage, the leaf blade proportion of the canopy and the length of the regrowth period of the sward might affect the concentration of fat, and its FA profile in the herbage. Regrowth period affected total FA concentration, and lower concentrations of linolenic and oleic acids occurred after a longer period of regrowth. N application resulted in higher concentrations of all FA, but the FA profile was not affected by N application. However, a longer regrowth period
210
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
Fig. 1. Intake of C18:3 (g/d) of two groups of 6 cows, stall-fed freshly cut perennial ryegrass of cultivars Barlet and Magella, cut daily at a herbage yield of circa 2000 kg DM/ha from June to September, and amount of CLA produced in their milk (g/d), during four sampling dates (Elgersma et al., 2003a).
decreased the proportion of linolenic acid and increased those of linoleic and palmitic acids. A strong positive overall linear relationship occurred between concentrations of total FA and linolenic acid with the N concentration of the herbage. These results were confirmed by further experiments (Witkowska et al., 2006). Lipids in plants are not static entities, but are continuously subject to turnover, meaning that lipid degradation is a normal process in the living plant and that lipases are normally present. Under normal growing conditions this will not have an important influence on the FA composition of the lipid fraction in plants. However, there are at least three times when the lipid fraction in plants, or plant parts, may significantly be modified, being senescence, after detachment (i.e., grazing or cutting) and during storage. In detached plants immediately after cutting, and perhaps during the early stages of ingestion and ensiling, metabolism of plant cells continues and there is still activity of the enzymes in detached and dying tissue. Continuation of processes of respiration and proteolysis are best known, but lipolysis also occurs. In ruminants grazing fresh pastures, the first stages of lipolysis in the rumen could be mediated by plant, rather than microbial, lipases (Lee et al., 2003a,b). Lipases are widely present in living plants and their regulation might be altered due to the double stress of elevated temperature and anoxia imposed on the metabolism of plant cells still intact after ensiling or ingestion by ruminants. Dewhurst and King (1998) studied effects of ensiling on the FA in the resulting silage. Wilting prior to ensiling reduced the content of total FA by almost 30%, with a reduction of up to 40% in linolenic acid. These authors suggested that ensiling has little influence, provided compaction and sealing of the silos is effective, which may not always be the case in ‘big bale’ silages. Adding silage additives, such as formic acid or formalin, substantially reduced losses, which was also noted for formic acid treatment (Doreau and Poncet, 2000). Reducing FA losses due to lipolysis and oxidation during wilting prior to conservation as silage are important strategies to manipulate precursors for CLA in milk.
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
211
Hay making reduced total FA by over 50%, with a higher loss of linolenic acid (Doreau and Poncet, 2000), similar to the loss in haylage (700 g DM/kg) (Elgersma et al., 2003c).
3. Fatty acid conversions in the rumen and mammary gland In contrast to short- and medium-chain FA, ruminants synthesise very little long-chain C18 FA that are desirable in milk. Thus, long-chain FA must be ingested in the feed if they are to be secreted into milk. Between 75% and 90% of linoleic, and 85% and 95% of linolenic, acids are biohydrogenated in the rumen (Kalscheur et al., 1997; Lock and Garnsworthy, 2002; Loor et al., 2004a). In herbage, linolenic acid predominates while maize contains mainly linoleic acid. Commonly used concentrate feed ingredients are often based on plant by-products and are low in fat. Some special ruminant feed products exist in which FA are protected against interference by rumen biohydrogenation (Itabashi and Baevre, 2001). A popular source of vegetable FA in such products is palm oil that is rich in saturated FA. More recently, inclusion in diets of full fat oil seeds high in PUFA has gained popularity. In most oil seeds, linoleic acid predominates as the major PUFA, but linseed contains mainly ␣-linolenic acid. Animal diets could also be supplemented with marine oils, containing predominantely FA of 20 or 22 carbons as the major FA, but this might negatively affect milk flavour, making plant sources, especially forage, the most environmentally sustainable source (Dewhurst et al., 2003a). There are a number of ways to increase the concentration of desired FA in ruminant food products, such as by increasing the amount (i.e., intake) or concentration of their precursors in the diet, by reducing the extent of biohydrogenation in the rumen, and/or by enhancing activity of the 9 —desaturase enzyme that converts vaccenic acid into rumenic acid in the udder. A varying proportion of PUFA, ranging from less than 2%, to over 20%, is recovered in milk as vaccenic acid, an important product of biohydrogenation of both linoleic and linolenic acids. There is a strong relationship between the contents of rumenic and vaccenic acids in cows milk, with the content of vaccenic acid being 2–2.5 times that of rumenic acid. In cows milk, about 70% of rumenic acid originates from conversion of vaccenic acid by 9 —desaturase in the mammary gland and other tissues (Griinari et al., 2000; Bauman et al., 2001). Lipolysis and biohydrogenation have been extensively studied in vitro, notably with soybean oil and, to a lesser extent, with linseed oil. The FA composition of linseed oil resembles that of fresh grass, in that lipids in fresh grass also contain a high proportion of linolenic acid. In experiments of Chow et al. (2004) with linseed oil, an accumulation of the intermediates C18:2 trans-11, cis-15 and vaccenic acid occurred. This was also observed in vivo in the rumen of cows fed linseed oil (Loor et al., 2004b). Because of the similarity in FA profile between fresh grass and linseed oil, the C18:2 trans-11, cis-15 is probably also an important intermediate in the rumen and a precursor for CLA in milk of grass-fed cows. It is likely that this is reflected in the FA profile of milk produced by grass-fed dairy cows. Research in our laboratory showed that, in grazing cows, the C18:2 trans-11 cis-15 content, when expressed as a proportion total FA, ranged between 5 and 8 g/kg FA, whereas on winter diets it never exceeded 1 g/kg FA.
212
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
4. Lipids in milk 4.1. Seasonal effects Milk fat is a mixture of FA, but this overview will focus on proportions of unsaturated fatty acids (UFA), n−3 FA, as well as concentrations of CLA and vaccenic acid, as these are the desired categories of FA in milk fat relative to human health. Seasonal variation in milk FA composition has long been recognized and several authors refer to Riel (1963) in this respect, although it seems to have been first reported by Mattsson (1949) who reported concentrations of conjugated dienoic acids of 6–24 g/kg (with one milk fat with 37 g/kg), and lower levels for stall-fed cows. In The Netherlands, Stadhouders and Mulder (1955) reported a three-fold difference in conjugated dienoic acid concentrations in milk of cows fed in stalls versus pastured (i.e., 7 versus 25 g/kg). Although conjugated dienoic acids include more FA than CLA, these early findings are consistent with recent data. Research in New Zealand (Auldist et al., 1998) and the UK (Lock and Garnsworthy, 2003) revealed seasonal variation in the CLA content of milk fat with highest concentrations, 12.7 and 17.0 g/kg fat, respectively, in grazing cows. Lowest concentrations were in winter and amounted to 6.0 g/kg fat both in New Zealand (Auldist et al., 1998) and the UK (Lock and Garnsworthy, 2003). There was no relationship between milk fat level and CLA proportion of fat. Seasonal fluctuations in milk CLA concentrations were recently measured in The Netherlands (Fig. 2). Nał˛ecz-Tarwacka (Habilitation (PhD Thesis), Warsaw University, Poland) studied 429 cows in 23 farms in central Poland over 2 years. The proportion of UFA was 344 g/kg fat in summer, when all cows were fed fresh grass, and 308 g/kg in winter when they were fed maize silage, grass silage and brewers’ grains. The n−3 FA declined from 9 to 8 g/kg, and the CLA concentration from 7.2 to 5.4 g/kg. In another study, Reklewska et al. (2003) reported CLA concentrations in milk of Black-and-White cows in Poland to be higher in summer (8.4 g/kg) and autumn (8.9 g/kg) versus winter (6.3 g/kg). They also compared
Fig. 2. Seasonal variation for concentration of CLA in Dutch milk (2001–2002) (modified from Ellen et al., 2003).
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
213
Table 1 CLA concentrations (g/kg of milk fat) of cows on different feeding systems in Poland, depending on the season (Reklewska et al., 2003) Feeding system
Summer
Winter
Indoor-pasture ecological Indoor-pasture conventional Indoor TMR
10.0 5.0 6.7
7.1 6.9 5.4
CLA in milk from cows fed a total mixed ration versus pasture and respective values were 6.1 and 11.7 g/kg. A further study compared seasonal changes in cows indoors, on three feeding systems (Table 1, Reklewska et al., 2003). For unknown reasons, and contrary to the general trend of lower CLA concentrations in winter, cows on a conventional indoorpasture system, common in Poland, had a higher value in winter, when no pasture was offered, versus summer when pasture was offered ad libitum. A fast response in CLA content in milk occurred when cows changed from winter feeding to pasture (Kelly et al., 1998), and vice versa (Elgersma et al., 2004a). This was confirmed in further studies where cows were housed and fed only maize silage from October 3, following unrestricted stocking (A. Elgersma, unpublished, Fig. 3). Outcomes were consistent with Chilliard et al. (2001) that the maximum effect is reached within about 5 days. Recent research of Shingfield et al. (2006) suggests that, when feeding fish oil or sunflower oil, this enhancement may not always be consistent, and may even decline with time after an initial increase. We are not aware of such a decline in animals on pasture. 4.2. Regional, farming system and feeding system effects Jensen (2002) and Precht and Molkentin (1995, 2000) have produced extensive reviews on the FA profiles of milk fat. A selection of their data, and others, is in Table 2, although this is not a complete review of available data. Contents of vaccenic acid are also included in Table 2 when available, and some of the data are based upon only 3–5 samples, and others upon more than 1000, notably the data from Germany. Thus, most cases only reflect
Fig. 3. Quick decline in CLA concentrations (g/kg fat) in milk of six cows during a 14-day transition period from grass (unrestricted grazing of perennial ryegrass until 3 October = day 0) to maize silage fed indoors in 2003 (Elgersma, unpublished data).
214
Table 2 CLA, rumenic acid and vaccenic acid contents (mg/g fat) in bulk milk fat Country and season or conditon
Total CLA min
max
mean
max
mean
min
max
1.0 4.9 1.9 1.0 3.6
10.5 18.9 11.9 18.9 13.3
3.5 14.5 8.5 3.5
19.6 44.3 17.3 44.3
4.2
9.3 28.7 17.8 17.2 19.8 9.3 19.2 15.5 8.0
6.0 6.0 7.0 6.6
20.0 44.0 29.0 9.2
4.2
10.3
15.5
9.8
22.5
4.5
3.0
8.2
10.6
7.9
17.0
9.2 7.6 8.7 9.5 7.4
5.2
14.4
5.9 8.2 2.1
9.9 11.1 15.6
3.6
38.1
10.3 8.7 9.4 14.1
6.0 8.5 6.3 5.6
14.0 8.9 16.7 18.2
4.1 9.2 6.4 3.7
2.0 3.0 3.0 2.9
7.0 25.0 12.0 4.5
3.4
2.8
The Netherlands, summer
6.9
4.6
10.9
6.5
The Netherlands, spring/autumn
4.7
3.0
8.5
UK Greece Italy Ireland
Ref.
min
Germany, barn Germany, pasture Germany, transition Germany, all The Netherlands The Netherlands, barn The Netherlands, pasture The Netherlands, transition The Netherlands, winter
Austria Belgium Denmark Spain France
Vaccenic acid
4.5 12.0 7.6 7.5 7.3
14.7 20.0 21.1 17.1 23.6 25.1 19.1 21.0 35.4
Precht and Molkentin (2000) Precht and Molkentin (2000) Precht and Molkentin (2000) Precht and Molkentin (2000) Precht and Molkentin (1995, 2000) Ellen et al. (2001) Ellen et al. (2001) Ellen et al. (2001) G. Ellen, NIZO Food Research, Ede, The Netherlands, personal communication G. Ellen, NIZO Food Research, Ede, The Netherlands, personal communication G. Ellen, NIZO Food Research, Ede, The Netherlands, personal communication Precht and Molkentin (2000) Precht and Molkentin (1995, 2000) Precht and Molkentin (1995, 2000) Precht and Molkentin (1995, 2000) Precht and Molkentin (2000) Precht and Molkentin (1995) Precht and Molkentin (1995, 2000) Precht and Molkentin (1995, 2000) Precht and Molkentin (1995, 2000) Precht and Molkentin (1995, 2000)
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
mean
Rumenic acid
8.7 16.1 23.6
4.6 17.1 4.3
3.4 12.5 3.2
5.5 23.4 7.8
6.7 5.6 8.1 15.0 21.8 11.0 14.0
14.8 7.0 13.0 18.0 7.0 8.0
11.0 18.0 26.0 14.0 22.0
4.5
3.4
6.4
21.1 36.6 51.0
52.8 16.4
18.0 32.0 42.0
42.7 13.1
25.0 42.0 58.0
73.0 26.5
Precht and Molkentin (1995, 2000) Precht and Molkentin (2000) Collomb et al. (2002) Collomb et al. (2002) Collomb et al. (2002) MacGibbon et al. (2001) MacGibbon et al. (2001) Lin et al. (1995) Jensen (2002) ˙ Zegarska and Kuzdzal-Savoie (1988) ˙ Zegarska and Kuzdzal-Savoie (1988)
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
Luxemburg Sweden Switzerland, lowlands Switzerland, mountains Switzerland, highlands New Zealand New Zealand, autumn, milk from 44 herds USA Canada Poland, pasture feeding Poland, indoor feeding
215
216
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
bulk milk from one season, whereas others give a detailed picture of several seasons or circumstances. Data for The Netherlands from Ellen et al. (2001) in Table 2 are raw milk samples from 18 dairy farms taken four times over a year in the four seasons. Data from G. Ellen, NIZO Food Research, Ede, The Netherlands, personal communication in Table 2 are samples from tankers of raw milk from the whole country once a month over 12 months. This difference in study design might explain the smaller variation in FA concentrations in the second study. Average concentrations of rumenic acid in bulk milk in most countries are 4–10 g/kg of fat (Table 2), and concentrations during pasture feeding are 2–3 times those during barn feeding. The highest concentrations of rumenic acid are in milk fat from Ireland, New Zealand and Switzerland, which probably relates to long periods of pasture feeding and, for Switzerland, to unique meadow grasses and herbs from the mountains and highlands. Data for milk from the Swiss mountains are consistent with rumenic acid concentrations in Italian cheese, produced from milk of cows grazing mountain pastures, a median rumenic acid content of 16.7 g/kg fat, compared with 7.1 g/kg fat in cheese from barn-fed cows (Innocente et al., 2002). Data in Table 2 also shows that there is a strong positive relationship between concentrations of rumenic and vaccenic acids in milk fat, with vaccenic acid concentrations being 2–2.5 times those of rumenic acid. Collomb et al. (2002) found large differences in milk FA patterns related to the altitude of mountain pastures. The lowland cows were fed maize and concentrate in the barn, as well as having access to pasture, whereas cows in the mountains (900–1210 m) and highland sites (1275–2120 m) were only on pasture. The increase in PUFA in milk fats from the lowland to the highland cows was mainly due to the increase in rumenic acid. Jahreis et al. (1997) compared conventional farming with high external inputs of fertiliser and concentrates, with or without grazing during summer, with low exernal input ecological farming with summer grazing. It was observed that organically produced milk had the highest contents of both CLA and vaccenic acids in its milk fat, especially during the May to September grazing period. The authors explained the differences by the different feeding strategies between the systems, and claimed that the ‘green’ feeds in organic farming were richer in PUFA than the silages and concentrates fed in conventional farming, that the grass/legume silages were richer in PUFA compared to maize silages, and indicated that rations higher in fibre cause specific rumen bacterial populations, as measured by a higher content of branched-chain FA in milk fat. In another comparison (Dewhurst, 2003c) bulk milk samples were obtained from 10 organic, and 8 conventional, dairy farms during winter. The most notable difference between the herd types was in annual milk production, reflecting very different levels of concentrate feeding. A covariance analysis showed that many of the differences in FA composition between organic and conventional milk were related to milk production level of the cows. However, after accounted for effects of milk yield, some effects of organic farming remained, which were probably the result of the different range of dietary ingredients used by organic farmers. It is not clear whether the higher concentrations of palmitic acid, and lower concentrations of stearic acid, in organic milk were a result of differences in dietary fat sources or effects of rumen fermentation patterns on de novo synthesis of FA (Dewhurst, 2003c). The higher concentration of linolenic acid in organic milk is consistent with recent observations of higher concentrations of this FA in milk produced from red or white clover
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
217
Fig. 4. Changes in the concentrations (g/kg fat) of rumenic, vaccenic and linolenic acids and saturated, monoand poly-unsaturated fatty acids (SFA, MUFA, PUFA) in milk of six cows that were stall-fed freshly cut perennial ryegrass from June to September, and after 1 month unrestricted stocking on a pasture with a more diverse botanic composition, from September to October (Elgersma et al., 2003d).
silages compared to milk produced from grass silage (Dewhurst et al., 2003b). With a low level of concentrate feeding, and red clover silage as sole forage, these authors showed concentrations of linolenic acid in milk to be three-fold those of the concentrations in milk from cows fed grass silage (Dewhurst et al., 2003b). In addition to the difference between fresh and conserved forage, there also seems to be an effect of grazing per se. The CLA content of milk from stall-fed cows on cut grass was lower than that in milk from cows that grazed grass, as occurred in an indirect comparison (Fig. 4) by Elgersma et al. (2003d). Indeed, cows on pasture (Dhiman et al., 1999a; Elgersma et al., 2004a) grazing lush fresh grass (Dewhurst et al., 2003a; Elgersma et al., 2003d; Khanal and Olson, 2004) at a high herbage allowance (Elgersma et al., 2004b; Fig. 5), produced milk with the highest concentrations of PUFA. A review of the effect of pasturing on the CLA content of milk is in Table 3 . 4.3. Animal and breed effects ˙ Zegarska et al. (2001) reported milk FA profiles in summer milk from pastured cows and found higher CLA concentrations for Polish red (11.9 g/kg) versus Black-and-White
218
Table 3 Polyunsaturated FA and CLA in milk of cows on pasture Treatment
Cows
DIMa
Code
Treatment
Milk (kg/d)
Fat (g/kg)
0 0
Control
10 5.0
101 48.0
Average
Control diets indoors STDEV
33.4 5.9
35.5 3.3
Jahreis et al. (1997)
1 2 3
350 1600 260
Year round Year round Year round
Pasture Indoor Ecological
Kelly et al. (1998) Lawless et al. (1998)
4 5
8 16
May Control
Pasture US Pasture + 3 kg concentrates
29.6 20.1
37.2 38.9
10.9 16.6
22.5 23.3
9.5 7.1
Dhiman et al. (1999a)
6 7 8
12 11 12
September September September
1/3 Pasture 2/3 Pasture All Pasture
24.5 17.5 14.5
35.1 36.4 33.7
8.9 14.3 22.1
42.7 27.1 14.0
8.1 14.6 20.2
Auldist et al. (1998)
9 10 11
17 18 13
43 118 220
Early Mid Late
Spring pasture NZ Spring pasture NZ Spring pasture NZ
18.5 14.3 11.7
42.2 45.3 46.3
9.7 11.1 12.7
12
10
133
June
27.5
32.3
7.2
18.2
7.1
0.078
13
10
133
June
Pasture Holsteins, C4 grass Pasture Jerseys, C4 grass
24.8
36.8
5.9
18.6
7.5
0.071
14 15 16 17 18
965 965 965 965 965
46.2 46.2 44.8 48.3 50.8
10.8 9.6 10.0 9.0 12.7
White et al. (2001)
Thomson and Van der Poel (2000)
59
November December January February March
Pasture NZ Pasture NZ Pasture NZ Pasture NZ Pasture NZ
CLA (g/kg FA) 4.4 1.1
C18:2 (g/kg FA) 27.0 5.7
C18:3 (g/kg FA) 4.7 2.0
6.1 3.4 8.0
t11-C18:1 (g/kg FA)
C14:1/C14
14.3 6.6
0.102 0.056
22.1 12.1 26.7 0.093 0.118
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
Experiment
6 6 6 6 6 6 6
June July July July/August August August Sept
Pasture NL, period 1 Pasture NL, period 2 Pasture NL, period 3 Pasture NL, period 4 Pasture NL, period 5 Pasture NL, period 6 Pasture NL, period 7
30.0 29.2 30.3 29.3 26.7 23.6 23.7
40.0 39.0 39.0 38.0 41.0 41.0 42.0
10.2 12.0 14.3 15.7 16.9 14.5 15.2
21.6 24.0 20.4 17.7 19.9 19.0 16.8
7.9 7.0 9.6 6.0 6.3 5.5 6.3
29.9 31.0 34.4 37.1 37.3 32.3 32.8
Elgersma et al. (2004a)
26
6
October
Pasture NL
19.7
43.7
24.3
10.4
8.9
46.2
Lock and Garnsworthy (2003)
27 28 29 30 31
45 45 45 45 45
May June July August Sept
Pasture UK Pasture UK Pasture UK Pasture UK Pasture UK
27.0 29.0 25.0 27.0 30.0
42.0 37.0 39.0 36.0 34.0
14.0 17.0 14.0 9.0 10.0
22.0 28.0 38.0 36.0 36.0
8.0 10.0 10.0 11.0 12.0
45.0 40.0 26.0 35.0 36.0
a DIM = Days in milk.
186 180 227 186 186
0.079 0.073 0.064 0.059 0.056
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
Elgersma et al. (2003a)
19 20 21 22 23 24 25
219
220
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
Fig. 5. Concentration of CLA (g/kg fat) in milk of two groups of six cows each with continuous stocking on perennial ryegrass pastures, after a week with a high herbage allowance (44 kg DM/d) (day 0), and 3.5 and 7 days after reducing the herbage allowance to 22 kg DM/d (Elgersma et al., 2004b).
(9.4 g/kg). Other authors (White et al., 2001; Kelsey et al., 2003) noted small, but significant, breed differences. Individual animal variation may also be important as cows fed the same diet had a threefold difference in milk conjugated linoleic acid (CLA) content (Kelsey et al., 2003). These authors found that breed (i.e., Holstein versus Brown Swiss), parity and lactation stage had little relationship to individual variation in milk fat content of CLA, and the CLA-desaturase index, and concluded that these CLA variables were essentially independent of milk yield, milk fat proportion and milk fat yield. Elgersma et al. (2004a) reported a range in CLA concentrations in milk of six grass grazed cows, of 14–36 g/kg of milk fat and 4.0–5.8 g/kg, at the end of a 2 weeks transition period to a 1:1 grass/maize silage diet. In a second experiment, the CLA contents in milk fat of 12 cows ranged from 12.4 to 27.8 g/kg on grazed grass, and from 4.0 to 8.6 g/kg 4 days after transition to maize silage. In general, CLA concentrations differed among cows, but patterns in response to diet changes were similar. The ranking of cows for the CLA content in their milk at the various sampling days was similar (Elgersma et al., 2004a), consistent with Lock and Garnsworthy (2003) who also found consistency in the ranking of individual cows in cis-9, trans-11 C18:2 content in milk fat with increased time on the same diet, or when cows changed diets. Provided the trait is at least moderately heritable, this could offer scope for selecting high CLA milk cows for breeding.
5. Trends and future perspectives During the last few decades, the FA composition of milk has become less favorable in The Netherlands as essential FA and CLA concentrations have declined. In the 1960s, summer Dutch farm milk contained, on average, 15 g/kg CLA (Elgersma, unpublished results), but
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
221
Fig. 6. Relationship between concentrations of CLA (g/kg fat) and unsaturated fatty acids (UFA) in milk of individual cows in two experiments with A. 6 cows (2000) and B. 12 cows (2002) during transition from unrestricted grazing to indoor feeding with silage (based on data from Elgersma et al., 2004a).
in 2001–2002 (Fig. 2) the average was 7 g/kg between June and August, and 5 g/kg in spring and autumn (Ellen et al., 2003). With low-fat dairy products being marketed, human intake of CLA is declining even further as ruminant food products are the main source of human CLA intake. Health effects of CLA need further study in humans, but the beneficial effect of unsaturated FA in general now seems commonly accepted. As CLA concentrations are correlated with those of unsaturated FA, they could perhaps be used as indicators of the FA composition milk (Fig. 6). The potential of plant breeding and management to increase the beneficial FA content of grass and clover species was recently reviewed by Dewhurst et al. (2003a). As fertilization and herbage allowance can be easily managed by farmers, it might be a feasible way to obtain higher concentrations of FA in herbage. As well, the timing of cutting or grazing (i.e., the regrowth stage at which herbage is harvested), can influence herbage quality.
222
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
The issues discussed in this review regarding the benefits of fresh herbage, and in particular grazing, could perhaps reverse the currently increasing trend for cows in The Netherlands to be kept indoors year round. However, effects on milk production, landscape values, animal welfare and public opinion will also play a role in the debate. Some economic analyses show benefits of grazing, depending on the farm size and spatial situation, as conserved feed is more expensive than fresh herbage (Van den Pol-van Dasselaar, 2005). However, cows with very high milk yield potential cannot meet their energy requirements from grass alone, partly due to insufficient intake (Taweel et al., 2005). Scollan et al. (2005) stated that grassland offers considerable scope to help create product differentiation in increasingly competitive markets. Farmers from a small Dutch dairy cooperative that produce milk from grazed grass now receive a premium payment in addition to the base milk price. A yoghurt producer buys milk from grazing dairies, pays the farmers a premium, and mentions the milk source in the product information for the consumer. In these cases, primary producers benefit from the higher market value at the end of the production chain. 6. Conclusions The FA profile of milk fat can be modified by feeding strategies, and there may be longer-term options by animal breeding. There are possibilities for a chain-approach from farm to processor to consumer, some examples were presented, and such an integrated approach is essential if scientific findings are to be put into practice. However, there remain questions about human health claims of various milk FA’s. Research, and standard protocols, for sampling, storage and FA analysis in forages are needed, and there is current research underway in this area in many parts of the world. References Aro, A., Mannisto, S., Salminen, I., Ovaskainen, M.L., Kataja, V., Uusitupa, M., 2000. Inverse association between dietary and serum conjugated linoleic acid and risk of breast cancer in post-menopausal women. Nutr. Cancer 38, 151–157. Ascherio, A., Rimm, E.B., Giovannucci, E.L., Spiegelman, D., Stampfer, M., Willett, W.C., 1996. Dietary fat and risk of coronary heart disease in men: cohort follow up study in the United States. Brit. Med. J. 313, 84–90. Auldist, M.J., Walsh, B.J., Thomson, N.A., 1998. Seasonal and lactational influences on bovine milk composition in New Zealand. J. Dairy Res. 65, 401–411. Banni, S., Angioni, E., Murru, E., Carta, G., Melis, M.P., Bauman, D., Dong, Y., Ip, C., 2001. TVA acid feeding increases tissue levels of conjugated linoleic acid and suppresses development of premalignant lesions in rat mammary gland. Nutr. Cancer 41, 91–97. Bauchart, D., V´erit´e, R., R´emond, B., 1984. Long-chain fatty acid digestion in lactating cows fed fresh grass from spring to autumn. Can. J. Anim. Sci. 64 (Suppl.), 330–331. Bauman, D.E., Corl, B.A., Baumgard, L.H., Griinari, J.M., 2001. Conjugated linoleic acid (CLA) and the dairy cow. In: Garnsworthy, P.C., Wiseman, J. (Eds.), Recent Advances in Animal Nutrition 2001. Nottingham University Press, Nottingham, UK, pp. 221–250. Belury, M.A., 2002. Dietary conjugated linoleic acid in health: physiological effects and mechanisms of action. Annu. Rev. Nutr. 22, 505–531. Boufa¨ıed, H., Chouinard, P.Y., Tremblay, G.F., Petit, H.V., Michaud, R., B´elanger, G., 2003. Fatty acids in forages. I. Factors affecting concentrations. Can. J. Anim. Sci. 83, 501–511.
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
223
Chilliard, Y., Ferlay, A., Doreau, M., 2001. Effect of different types of forages, animal fat or marine oils in cow’s diet on milk fat secretion and composition, especially conjugated linoleic acid (CLA) and polyunsaturated fatty acids. Livest. Prod. Sci. 70, 31–48. Chow, T.T., Fievez, V., Moloney, A.P., Raes, K., Demeyer, D., DeSmet, S., 2004. Effect of fish oil on in vitro rumen lipolysis, apparent biohydrogenation of linoleic and linolenic acid and accumulation of biohydrogenation intermediates. Anim. Feed Sci. Tech. 117, 1–12. Collomb, M., B¨utikofer, U., Sieber, R., Jeangros, B., Bosset, J.-O., 2002. Composition of fatty acids in cow’s milk fat produced in the lowlands, mountains and highlands of Switzerland using high-resolution gas chromatography. Int. Dairy J. 12, 649–659. Corl, B.A., Barbano, D.M., Bauman, D.E., Ip, C., 2003. Cis-9 trans-11 CLA derived endogenously from trans-11 18:1 reduces cancer risk in rats. J. Nutr. 133, 2893–2900. Dewhurst, R.J., King, P.J., 1998. Effects of extended wilting, shading and chemical additives on the fatty acids in laboratory grass silages. Grass Forage Sci. 53, 219–224. Dewhurst, R.J., Scollan, N.D., Lee, M.R.F., Ougham, H.J., Humphreys, M.O., 2003a. Forage breeding and management to increase the beneficial fatty acid content of ruminant products. Proc. Nutr. Soc. 62, 329–336. Dewhurst, R.J., Fisher, W.J., Tweed, J.K.S., Wilkins, R.J., 2003b. Comparison of grass and legume silages for milk production. 1. Production responses with different levels of concentrate. J. Dairy Sci. 86, 2598–2611. Dewhurst, R.J., 2003c. Fatty Acids in Milk Fat from Organic Dairy Farms. Elm Farm Research Centre Bulletin. Elm Farm Research Centre, Hamstead Marshall, Newbury, Berks, UK, p. 11. Dhiman, T.R., Anand, G.R., Satter, D., Pariza, M.W., 1999a. Conjugated linoleic acid content of milk from cows fed different diets. J. Dairy Sci. 82, 2146–2156. Dhiman, T.R., Helmink, D., McMahon, D.J., Fife, R.L., Pariza, M.W., 1999b. Conjugated linoleic acid content of milk and cheese from cows fed extruded oilseeds. J. Dairy Sci. 82, 412–419. Doreau, M., Poncet, C., 2000. Ruminal biohydrogenation of fatty acids originating from fresh or preserved grass. Repr. Nutr. Dev. 40, 201. Elgersma, A., Ellen, G., Dekker, P.R., van der Horst, H., Boer, H., Tamminga, S., 2003a. Effects of perennial ryegrass (Lolium perenne) cultivars with different linolenic acid contents on milk fatty acid composition. Asp. Appl. Biol. 70, 107–114. Elgersma, A., Ellen, G., van der Horst, H., Muuse, B.G., Boer, H., Tamminga, S., 2003b. Influence of cultivar and cutting date on the fatty acid composition of perennial ryegrass. Grass Forage Sci. 58, 323–331 (also Erratum Grass Forage Sci. 59, 104). Elgersma, A., Ellen, G., van der Horst, H., Muuse, B.G., Boer, H., Tamminga, S., 2003c. Comparison of the fatty acid composition of fresh and ensiled perennial ryegrass (Lolium perenne L.), affected by cultivar and regrowth interval. Anim. Feed Sci. Tech. 108, 191–205. Elgersma, A., Tamminga, S., Ellen, G., 2003d. Comparison of the effects of grazing and zero-grazing of grass on milk fatty acid composition of dairy cows. Grassl. Sci. Eur. 8, 271–274. Elgersma, A., Ellen, G., van der Horst, H., Muuse, B.G., Boer, H., Tamminga, S., 2004a. Quick changes in milk fat composition after transition from fresh grass to a silage diet and effects on consumer health benefits. Anim. Feed Sci. Tech. 117, 13–27. Elgersma, A., Ellen, G., Tamminga, S., 2004b. Rapid decline of contents of beneficial omega-7 fatty acids in milk from grazing cows with decreasing herbage allowance. Grassl. Sci. Eur. 9, 1136–1138. Elgersma, A., Maudet, P., Witkowska, I.M., Wever, A.C., 2005. Effects of N fertilization and regrowth period on fatty acid concentrations in perennial ryegrass (Lolium perenne L.). Ann. Appl. Biol. 147, 145–152. Ellen, G., te Giffel, M., Slaghuis, B., 2001. Invloed van melkveevoeding op de vetzuursamenstelling van melk. Zuivelzicht 93, 26–27. Ellen, G., te Giffel, M., Sprong, M., 2003. Be¨ınvloeding vetzuursamenstelling van melk via voer. Voedingsmagazine 16, 12–17. Griinari, J.M., Corl, B.A., Lacy, S.H., Chouinard, P.Y., Nurmela, K.V.V., Bauman, D.E., 2000. Conjugated linoleic acid is synthesized endogenously in lactating dairy cows by 9 desaturase. J. Nutr. 130, 2285–2291. Grundy, S.M., Vega, G.L., 1998. Plasma cholesterol responsiveness to saturated fatty acids. Am. J. Clin. Nutr. 47, 822–824. Havel, R.J., 1997. Milk fat consumption and human health: recent NIH and other American governmental recommendations. In: Welch, R.A.S., Burns, D.J.W., Davis, S.R., Popay, A.I., Prosser, C.G. (Eds.), Milk Composition, Production And Biotechnology. CAB International, Wallingford, UK, pp. 13–22.
224
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
Hawke, J.C., 1973. Lipids. In: Butler, G.W., Bailey, R.W. (Eds.), Chemistry and Biochemistry of Herbage. Academic Press, London, UK, pp. 213–263. Innocente, N., Praturlon, D., Corradini, C., 2002. Fatty acid profile of cheese produced with milk from cows grazing on mountain pastures. Ital. J. Food Sci. 14, 217–224. Ip, C., Banni, E., Carta Angioni, G., McGinley, J., Thompson, H.J., Barbano, D., Bauman, D., 1999. Conjugated linoleic acid-enriched butter fat alters mammary gland morphogenesis and reduces cancer risk in rats. J. Nutr. 129, 2135–2142. Itabashi, H., Baevre, L., 2001. Trends in milk composition: results of a survey by IDF. Bull. Int. Dairy Fed. 366, 9–14. Jahreis, G., Fritsche, J., Steinhart, H., 1997. Conjugated linoleic acid in milk fat: high variation depending on production system. Nutr. Res. 17, 1479–1484. Jensen, R.G., 2000. Invited review: the composition of bovine milk lipids. J. Dairy Sci. 85, 295–350. Kalscheur, K.F., Teter, B.B., Piperova, L.S., Erdman, R.A., 1997. Effect of dietary forage concentration and buffer addition on duodenal flow of trans-C18:1 fatty acids and milk fat production in dairy cows. J. Dairy Sci. 80, 2104–2114. Kelly, M.L., Kolver, E.S., Bauman, D.E., Amburgh, M.E., van, Muller, L.D., 1998. Effect of intake of pasture on concentrations of conjugated linoleic acid in milk of lactating cows. J. Dairy Sci. 81, 1630–1636. Kelsey, J.A., Corl, B.A., Collier, R.J., Bauman, D.E., 2003. The effect of breed, parity, and stage of lactation on conjugated linoleic acid (CLA) in milk fat from dairy cows. J. Dairy Sci. 86, 2588–2597. Kennelly, J.J., 2001. The fatty acid composition of milk fat as influenced by feeding oilseeds. Bull. Int. Dairy Fed. 366, 28–36. Khanal, R.C., Olson, K.C., 2004. Factors affecting conjugated linolenic acid (CLA) content in milk, meat, and egg: a review. Pakistan J. Nutr. 3, 82–98. Lavillonni`ere, F., Martin, J.C., Bougnoux, P., S´eb´edio, J.-L., 1998. Analysis of conjugated linoleic acid isomers and content in French cheeses. J. Am. Oil Chem. Soc. 75, 343–352. Lawless, F., Murphy, J.J., Harrington, D., Devery, R., Stanton, C., 1998. Elevation in conjugated cis-9, trans-11 octadecadienoic acid in bovine milk because of dietary supplementation. J. Dairy Sci. 81, 3259–3267. Lee, M.R.F., Harris, L.J., Dewhurst, R.J., Merry, R.J., Scollan, N.D., 2003a. The effect of clover silages on long-chain fatty acid rumen transformations and digestion in beef steers. Anim. Sci. 76, 491–501. Lee, M.R.F., Winters, A.L., Scollan, N.D., Dewhurst, R.J., Theodorou, M.K., Minchen, F.R., 2003b. Plant-mediated lypolysis and proteolysis in red clover with different polyphenol exidase activities. J. Sci. Food Agric. 84, 1639–1645. Lin, H., Boylston, T.D., Chang, M.J., Luedecke, L.O., Shultz, T.D., 1995. Survey of the conjugated linoleic acid contents of dairy products. J. Dairy Sci. 78, 2358–2365. Lock, A.L., Garnsworthy, P.C., 2002. Independent effects of dietary linoleic and linolenic fatty acids on the conjugated linoleic acid content of cow’s milk. Anim. Sci. 74, 163–176. Lock, A.L., Garnsworthy, P.C., 2003. Seasonal variation in milk conjugated linoleic acid and Δ9 —desaturase activity in dairy cows. Livest. Prod. Sci. 79, 47–59. Lock, A.L., Corl, B.A., Barbano, D.M., Bauman, D.E., Ip, C., 2004. The anticarcinogenic effect of trans-11 18:1 is dependent on its conversion to cis-9, trans-11 CLA by Δ9 —desaturase in rats. J. Nutr. 134, 2698– 2704. Loor, J.J., Ueda, K., Ferlay, A., Chilliard, Y., Doreau, M., 2004a. Biohydrogenation, duodenal flow, and intestinal digestibility of trans fatty acids and conjugated linoleic acids in response to dietary forage:concentrate ratio and linseed oil in dairy cows. J. Dairy Sci. 87, 2472–2485. Loor, J.J., Ueda, K., Ferlay, A., Chilliard, Y., Doreau, M., 2004b. Diurnal profiles of conjugated linoleic acids and trans fatty acids in ruminal fluid from cows fed a high concentrate diet supplemented with fish oil, linseed oil, or sunflower oil. J. Dairy Sci. 87, 2468–2471. MacGibbon, A.K.H., Van der Does, Y.E.H., Fong, B.Y., Robinson, N.P., Thomson, N.A., 2001. Variations in the CLA content of New Zealand milkfat. Aust. J. Dairy Technol. 56, 158. Mattsson, S., 1949. Poly-unsaturated fatty acids in butter and their influence on the oxidation of butter. Methods of analysis and preliminary results. In: Proceedings of the XIIth International Dairy Congress, Stockholm, pp. 308–324, Section II. Nał˛ecz-Tarwacka, T. Effect of selected factors on the functional component of milk fat in dairy cows. Habilitation (PhD Thesis), Warsaw University, Poland, Submitted for publication.
A. Elgersma et al. / Animal Feed Science and Technology 131 (2006) 207–225
225
Precht, D., Molkentin, J., 1995. Trans fatty acids: implications for health, analytical methods, incidence in edible fats and intake. Die Nahrung 39, 343–374. Precht, D., Molkentin, J., 2000. Frequency distributions of conjugated linoleic acid and trans fatty acid contents in European bovine milk fats. Michwissenschaft 55, 687–691. Reklewska, B., Bernatowicz, E., Reklewski, Z., Nał˛ecz-Tarwacka, T., Kuczy´nska, B., Zdziarski, K., Oprz˛adek, A., 2003. Concentration of milk functional components in Black-and-White cows, depending on the season and feeding system (in Polish). Zeszyty Naukowe Przegl˛adu Hodowlanego 68, 85–98. Riel, R.R., 1963. Physico-chemical characteristics of Canadian milk fat. Unsaturated fatty acids. J. Dairy Sci. 46, 102–106. Salminen, I., Mutanen, M., Jauhiainen, M., Aro, A., 1998. Dietary trans fatty acids increases conjugated linoleic acid levels in human serum. Nutr. Biochem. 9, 93–98. Santora, J.E., Palmquist, D.L., Roehrig, K.L., 2000. Trans-vaccenic acid is desaturated to conjugated linoleic acid in mice. J. Nutr. 130, 208–215. Scollan, N.D., Dewhurst, R.J., Moloney, A.P., Murphy, J.J., 2005. Improving the quality of products from grassland. In: McGilloway, D.A. (Ed.), Grassland: a global resource. Wageningen Academic Publishers, Wageningen, The Netherlands, pp. 41–56. Shingfield, K.J., Reynolds, C.K., Hervas, G., Griinari, J.M., Grandison, A.S., Beever, D.E., 2006. Examination of the persistency of milk fatty acid composition responses to fish oil and sunflower oil in the diet of dairy cows. J. Dairy Sci. 89, 714–732. Stadhouders, J., Mulder, H., 1955. The composition of Dutch butterfat. 1. Seasonal variations in the unsaturated fatty acid composition of butter fat. Neth. Milk Dairy J. 9, 182–193. Tamminga, S., 2001. Effects of feeds, feed composition and feed strategy on fat content and fatty acid composition in milk. Bull. Int. Dairy Fed. 366, 15–24. Taweel, H.Z., Tas, B.M., Smit, H.J., Elgersma, A., Dijkstra, J., Tamminga, S., 2005. Effects of feeding perennial ryegrass with an elevated concentration of water-soluble carbohydrates on intake, rumen function and performance of dairy cows. Anim. Feed Sci. Technol. 121, 243–256. Thomson, N.A., Van der Poel, W., 2000. Seasonal variation of the fatty acid composition of milk fat from Friesian cows grazing pasture. Proc. NZ Soc. Anim. Prod. 60, 314–317. Turpeinen, A.M., Mutanen, M., Aro, A., Salminen, I., Basu, S., Palmquist, D.L., Griinari, J.M., 2002. Bioconversion of vaccenic acid to conjugated linoleic acid in humans. Am. J. Clin. Nutr. 76, 504–510. Van den Pol-van Dasselaar, A., 2005. Grazing in transition (in Dutch). Animal Sciences Group, Lelystad, The Netherlands. PraktijkRapport Rundvee 81, 127. White, S.L., Bertrand, J.A., Wade, M.R., Washburn, S.P., Green Jr., J.T., Jenkins, T.C., 2001. Comparison of fatty acid content of milk from Jersey and Holstein cows consuming pasture or a total mixed ration. J. Dairy Sci. 84, 2295–2301. Williams, C.M., 2000. Dietary fatty acids and human health. Ann. Zootech. 49, 165–180. Witkowska, I.C., Wever A.C., Elgersma A., 2006. Seasonal effects on fatty acid concentrations in perennial ryegrass (Lolium perenne L.) in relation to nitrogen and regrowth interval. Eur. J. Agron, Submitted for publication. ˙ Zegarska, A., Jaworski, J., Paszczyk, B., Charkiewicz, J., Borejszo, Z., 2001. Fatty acid composition with emphasis on trans C18:1 isomers of milk fat from lowland Black-and-White and Polish Red cows. Pol. J. Food Nutr. Sci. 4, 41–44. ˙ Zegarska, Z., Kuzdzal-Savoie, 1988. Seasonal effects on the fatty acids content in milk fat. Michwissenschaft 43, 777–779.