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Influence of breed on bovine milk cis-9, trans-11-conjugated
linoleic acid content
a a b c b b ,
*
F. Lawless , C. Stanton , P. L’Escop , R. Devery , P. Dillon , J.J. Murphy
a
Teagasc, Dairy Products Research Centre, Moorepark, Fermoy, Co. Cork, Ireland
b
Teagasc, Dairy Production Research Centre, Moorepark, Fermoy, Co. Cork, Ireland
c
School of Biotechnology, Dublin City University, Dublin, Ireland
Received 16 July 1998; received in revised form 2 March 1999; accepted 10 March 1999
Abstract
The influence of animal breed on the profile of fatty acids in milk and particularly on the concentration of cis-9, trans-11 octadecadienoic acid, a conjugated lineoleic acid (CLA) was investigated using four breeds of cows, Irish Holstein / Friesian
(IH, n523), Dutch Holstein / Friesian (DH, n522), Montbeliardes (MB, n529) and Normandes (NM, n527), on pasture.
All cows were grazed together in one group. Milk fat CLA concentration from MB were significantly higher (P,0.05) than
from DH at one of the two sampling times, while the CLA content of milk fat from NM, IH and DH was not significantly different at either sampling time. Milk fat CLA concentrations between the four breeds ranged from 14.7 to 18.6 mg / g fat, while the variation in milk fat CLA between individual cows within the four breeds ranged from 4.8 to 35.6 mg / g fat. There
were significant correlations between milk fat CLA concentrations of individual cows within NM (P,0.001), MB
(P,0.001) and IH (P,0.001) and the correlation was close to being significant for DH cows (P50.076) at two sampling
dates. In terms of total fatty acid profiles, DH had higher (P,0.05) C16:0 concentrations than the other breeds. The IH had a
higher (P,0.05) C16:0than the MB. The C18:0content was higher (P,0.05 at least) in milk fat from NM and MB than
from DH and total C18:1concentrations were close to being significantly higher (P50.067) in the MB than in the IH. The
data indicate that animal breed has some influence over the CLA content of milk and that cows yielding high levels of milk fat CLA sustain this production over time. While there were some significant differences between the breeds in the concentrations of C16:0, C18:0 and C18:1 it is unlikely that they are large enough to be of practical importance. 1999 Elsevier Science B.V. All rights reserved.
Keywords: Conjugated lineolic acid; Fatty acid profile; Breed
1. Introduction containing products and reduced cancer risk (Jar-vinen et al., 1997; Knekt et al., 1996), pointing Epidemiological studies suggest a link between toward the existence of anticarcinogenic compounds increased dietary intakes of meat and dairy-fat in animal and milk fats. Conjugated linoleic acid (CLA) is a fatty acid which is recently the focus of much interest due to its many attributed beneficial *Corresponding author. Tel.: 1353-25-42222; fax: 1
353-25-effects. These include anticarcinogenic activity (Bel-42340.
E-mail address: [email protected] (J.J. Murphy) ury, 1995; Ha et al., 1990; Ip et al., 1991; 1994;
Parodi, 1994; Shultz et al., 1992) and inhibition of of .99% purity) and anhydrous Na SO2 4 (ASC development of atherosclerosis in animals (Lee et al., reagent 99.7% purity) were obtained from Sigma (St. 1994; Nicolosi et al., 1993; Nicolosi and Laitinin, Louis, MO, USA). CLA standard was a gift provided 1996), in addition to a role as growth promoter (Chin by Dr. M. Pariza of The Food Research Institute et al., 1994), the ability to reduce the catabolic (University of Wisconsin, Madison, WI, USA). Hex-effects of immune stimulation (Cook et al., 1993; ane, methanol and chloroform were HPLC grade and Miller et al., 1994) and ability to reduce body fat were obtained from Lab-Scan Analytical Sciences (Pariza et al., 1996). CLA (cis-9, trans-11 isomer) is (Stillorgan, Co. Dublin, Ireland). Methanolic-HCl produced naturally in the rumen as an intermediate was obtained from Supelco (Bellefonte, PA, USA) during the biohydrogenation of dietary linoleic to and KOH AnalaR grade was obtained from Prolabo stearic acid and it is also this isomer which has been (Manchester, UK).
implicated as the most biologically active. The principal dietary sources of the cis-9, trans-11 CLA isomer include animal-fat containing foods, such as
2.2. Animal breeds beef, lamb, milk and dairy products (Chin et al.,
1992). Current estimates of the average daily intake
Milk samples were obtained from four different of CLA range from 0.35 to ¯1 g (Chin et al., 1992;
breeds on pasture. Irish Holstein / Friesians (IH, n5 Fritsche and Steinhart, 1998) while a daily intake of
23) had an average RBI95 (relative breeding index)
¯3 g is predicted to provide protection against
of 110. Dutch Holstein / Friesians (DH, n522) cancer (Ip et al., 1994).
imported into Ireland from the Netherlands had an A number of factors have been shown to influence
average RBI95 of 130. Montbeliardes (MB, n529) the levels of CLA in bovine milk fat, including
and Normandes (NM, n527) were imported from animal age (Lal and Narayanan, 1984; Stanton et al.,
France and had been selected from some of the 1997a), dietary restriction (Jiang et al., 1996), feed
higher genetic merit animals of the breeds in France. allowance (Lawless et al., 1996; Stanton et al.,
The animals were assembled between November 1997a), seasonal variation (Riel, 1963; Parodi, 1977;
1995 and January 1996 as in-calf heifers. These Stanton et al., 1997b) and dietary oils (Dhiman et al.,
animals were the product of 10, 14, 8 and 10 sires in 1996; 1997; Kelly and Bauman, 1996; Lawless et al.,
the IH, DH, MB and NM breeds, respectively and all 1996; Stanton et al., 1997a; Lawless et al., 1998). It
had different dams. There were no animals with has been shown that breed of animal affects the fatty
common sires in the IH and DH breeds. This study acid composition of intramuscular fat (Siebert et al.,
was carried out in 1997 when all the animals were in 1996) and milk fat (Beaulieu and Palmquist, 1995)
their second lactation. All cows were grazed together but CLA was not measured in these studies. As far
in one group and their diet consisted of grazed grass as can be determined there are no published data on
only. the CLA content of milk from different breeds of
cattle. An ongoing study evaluating the biological
and economic efficiency of a number of breeds on a 2.3. Collection of milk samples pasture-based system of milk production (Dillon et
al., 1998) afforded the opportunity of obtaining milk Milk samples from individual cows at pasture samples with the objective of determining the CLA were taken on two occasions, by sampling from the content as well as the total fatty acid profiles of the recording jars in the milking parlour after agitation at
milk fat. the evening milking. Evening (p.m.) milk samples
were used as they contain a higher percentage of fat compared to morning milk samples. The samples 2. Materials and methods were stored at 2208C before extraction of the fat. The mean calving dates for the IH, DH, MB and NM
2.1. Reagents cows were March 8, March 6, March 13 and March
and 115 and 71 and 116 for the four breeds, flow-rate was 300 ml / min. The injector temperature
respectively. was 2008C and the detector temperature was 2508C.
The chromatograph was programmed from 808C, 2.4. Milk yield and composition with an initial delay time of 2 min, at a rate of 168C / min during each analysis and held at a final Milk yield was measured on 4 days in the week of temperature of 2008C until all the fatty acids were sampling in order to determine the relative pro- eluted. Fatty acids were identified by their retention duction of the herds. Milk composition (fat, protein times with reference to standard FAMEs and peak and lactose) was determined on one successive areas were computed using a Trilab 2000 micro-morning and evening sample taken in that week by computer (Trivector Scientific, Turvey, Bedford, automated infrared analysis using a Milkoscan 605 UK). The response factors of the individual fatty (Foss Electric, Hillerod, Denmark). acids were calculated relative to the area of C16:0 which was assigned a response factor of 1.00. Fatty 2.5. Quantification of milk fat CLA and trans-11- acids were expressed as g / 100 g fatty acids. C18:1 content
2.6. Statistical analysis Milkfat samples were obtained from whole milk
by centrifugation, as described by Murphy et al. Milk yield, constituent yield and composition, (1990). The triglyceride and free fatty acid forms of milk CLA and milk fat individual fatty acid data CLA (cis-9, trans-11 isomer) and the trans-11-C18:1 were analysed using the GLM procedure ofSAS(SAS isomer in milk fat from individual cows were Institute, Cary, NC, USA, Version 6.12) taking out quantified by gas–liquid chromatography (GLC), breed effects only. Samples from every animal were using a Varian 3500 GLC (Varian, Harbor City, CA, not available for all analyses and thus, the number of USA) fitted with a flame ionisation detector (FID), samples per breed for CLA analysis at the first according to the method of Chin et al. (1992) using sampling time were 20, 20, 29 and 25 and at the acid-catalysed methanolysis, as previously described second sampling time were 23, 22, 29 and 27. For (Stanton et al., 1997a; Lawless et al., 1998), with individual fatty acid analysis sample numbers were reference to the internal standard C13:0. The cis-9, 18, 15, 27 and 25 from the IH, DH, MB and NM trans-11 CLA isomer in milk fat samples was breeds, respectively. Correlation of milk fat CLA identified by retention time with reference to a CLA content at sampling time one and sampling time two mix, generously provided by The Food Research (Proc Corr inSAS) was performed on 20, 20, 29 and Institute, University of Wisconsin (Madison, WI, 25 animals in the IH, DH, MB and NM breeds, USA). The trans-11-C18:1 isomer was identified by respectively.
retention time with reference to standard trans-11-C18:1 FAME (Sigma, St. Louis, MO, USA), as
described by Lawless et al. (1998). 3. Results and discussion
2.6. Quantification of fatty acid methyl esters in The production characteristics of the four breeds
milk fat during the period of milk sampling are reported in
sig-Table 1
Milk yield and milk composition of the four breeds in the weeks of both samplings
a
Sampling Holstein / Friesians Montbeliardes Normandes SED
Irish (IH) Dutch (DH)
Milk (kg / day) 1 24.3 28.1 26.1 23.5 1.30
2 19.8 23.2 20.7 19.2 0.99
Fat (g / kg) 1 33.5 37.2 36.8 36.9 2.16
2 33.4 37.2 35.9 36.7 1.43
Fat (g / day) 1 792 1034 964 867 67.1
2 663 854 747 704 42.3
Protein (g / kg) 1 33.1 34.0 33.7 34.8 0.64
2 33.4 34.5 34.4 35.7 0.71
Protein (g / day) 1 783 952 873 814 41.1
2 655 794 711 681 28.3
Lactose (g / kg) 1 47.7 47.6 48.6 49.3 0.40
2 45.4 45.8 46.5 47.1 0.37
Lactose (g / day) 1 1141 1337 1267 1160 45.9
2 901 1066 964 906 33.3
a
Standard error of difference.
nificantly higher than that of the IH cows (P,0.01). content of the MB cows was highest at 18.3 mg / g The DH cows had the highest fat yield and this was fat, while the DH cows yielded the lowest content of significantly higher than that of the IH (P,0.001) or CLA in the milk fat (14.7 mg / g fat) of the breeds the NM cows (P,0.05). The DH cows also pro- examined. The milk fat CLA content of MB cows duced a higher yield of protein than the other three was significantly (P,0.05) higher than that of the breeds (P,0.001 for IH, P,0.01 for NM and DH cows and although proportionally 0.18 higher
P50.058 for MB). than NM cows, it was not significant (P50.089).
At the second sampling time the DH cows were The higher milk fat CLA content of MB cows, producing higher milk yields than the other three compared to the other breeds examined, observed at breeds (P,0.05 at least). The IH cows had a lower the first sampling was sustained at the second milk fat concentration than the DH (P,0.05) or the sampling. MB cows produced on average, 18.6 mg NM cows (P,0.05). The NM cows again had a CLA / g fat at the second sampling, which was significantly higher protein concentration (P,0.01) similar to the level obtained at the first sampling. than the IH cows. The milk fat and protein yields of Also, of the four breeds, the lowest level of milk fat the DH cows were significantly higher than that of CLA was again obtained from the DH cows. How-the oHow-ther three breeds (P,0.05 at least). ever, at the second sampling, the difference between The average CLA content of milk obtained from the milk fat CLA content of MB and DH cows was the four breeds at both sampling times is shown in not statistically significant (P50.26).
Table 2. At the first sampling time milk fat CLA In order to determine if expressing CLA per kg of
Table 2
CLA content of the milks from the different breeds at the two sampling times
a
Sample CLA (mg / g fat and mg / kg milk) SED
Holstein / Friesian Montbeliardes Normandes
(MB) (NM)
Irish (IH) Dutch (DH)
1 17.0, 560.7 14.7, 529.0 18.3, 668.5 15.5, 573.7 1.71, 71.3
2 17.9, 580.0 16.7, 614.9 18.6, 651.7 17.2, 627.4 1.69, 58.3
a
milk compared to the more common mg / g fat had an 18.6 mg / g fat at the second sampling time), the effect on the differences between breeds, the CLA variation in milk fat CLA content among individual content in mg / kg milk in the different breeds was cows within each of the breeds was much higher. compared. The CLA data given in mg / kg milk were Within the IH cows, the CLA content of milk fat obtained by multiplying the CLA in mg / g fat by the ranged from 7.8 to 31.5 mg / g fat, for the DH cows fat content in g / kg milk. At the first sampling, MB the range was 4.8 to 27.0 mg / g fat, for MB cows cows yielded higher (P50.053) CLA / kg milk than CLA content ranged from 4.9 to 35.6 mg / g fat and the DH cows, similar to the trend obtained for CLA for NM cows the range was 5.6 to 29.8 mg / g fat. content, expressed as mg / g fat. The yields of CLA / This large variation in the CLA content of milk of kg milk obtained from IH, MB and NM cows were individual cows is now well documented (Jiang et not significantly different. At the second sampling, al., 1996; Stanton et al., 1997a; Lawless et al., 1998). MB cows again yielded the highest CLA content The total fatty acid profiles of the milk fat from when expressed as mg / kg milk but there were no the four breeds is shown in Table 4. In general, milk significant differences between any of the breeds at fat from the MB and the NM cows had lower this sampling. Therefore, the yield of CLA in milk, concentrations of C16:0 and higher concentrations of expressed as mg / g fat, followed similar trends to C18:0 and C18:1 than the IH or DH cows. The yields of CLA / kg milk, among the four breeds concentration of C16:0 was significantly lower in
studied. milk fat from MB cows compared with milk fat from
The correlation coefficients between the milk fat DH (P,0.001) and IH (P,0.05) cows. NM cows CLA contents from the first and the second sam- had a significantly lower (P,0.01) milk fat C16:0 plings for individual cows in each breed are shown concentration compared with DH cows. Conversely, in Table 3. The correlation coefficients were statisti- total C18:1 concentration in milk fat tended to be cally significant (P,0.001) for IH, MB and NM and higher for MB than for IH cows (P50.067). The close to significant (P50.076) for DH cows, in- C18:0 concentration of milk fat was significantly dicating that cows maintain their individual level of higher for the NM compared to the DH (P,0.01) milk fat CLA production over time, at least within cows. Little data are available on breed differences one lactating season. These findings may suggest that in the composition of milk fat but those which do individual cows producing very high levels of CLA exist suggest that breed does influence the fatty acid sustain this throughout the lactating season, and profiles. Both Stull and Brown (1964) and Palmquist possibly also from year to year. However, further and Beaulieu (1992) observed that cows of the confirmatory data are required. The data from both Holstein breed had significantly higher levels of time points were also analysed statistically for a C18:1 than cows of the Jersey breed. Holsteins also relationship between milk fat CLA content, milk fat had lower levels of C –C6 14 fatty acids than Jerseys. content and milk yield. There was no significant The correlation coefficient between the concen-correlation between the CLA content of milk and tration of trans-11-C18:1 and CLA was determined milk fat content or milk yield. and found to be highly significant (R50.785, P5 Although the ranges in the averages of the milk fat 0.0001). We have previously observed a strong CLA contents for each breed were small (14.7 to positive correlation between these two fatty acids 18.3 mg / g fat at the first sampling time and 16.7 to (Lawless et al., 1998) confirming the earlier findings
Table 3
Correlation coefficients between the CLA contents (mg / g fat) of the individual cows within breeds at the first and second samplings
Holstein / Friesian Montbeliardes Normandes
(MB) (NM)
Irish (IH) Dutch (DH)
R 0.75 0.41 0.74 0.63
Table 4
Concentrations of the individual fatty acids in the milk fat of the four breeds
a
Fatty acid Concentration (g / kg total fatty acids) SED
Holstein / Friesian Montbeliardes Normandes
(MB) (NM)
Irish (IH) Dutch (DH)
C4:0 10.1 10.9 10.3 10.6 0.37
C6:0 11.9 11.8 11.5 11.9 0.38
C8:0 10.5 9.8 9.9 10.3 0.41
C10:0 28.9 25.8 27.6 28.2 1.45
C10:1 2.6 2.4 2.0 2.4 0.15
C12:0 36.5 32.5 34.6 36.0 1.88
C12:1 0.8 0.7 0.6 0.7 0.06
C14:0 108.5 107.2 110.0 109.2 3.75
C14:1 9.1 8.9 6.4 8.0 0.69
C16:0 241.1 257.7 228.1 236.7 6.30
C18:0 111.5 103.8 115.1 119.3 4.41
C18:1trans 58.2 53.0 57.7 54.5 5.08
C18:1total 261.1 262.3 276.4 265.9 8.5
C18:2 10.7 10.1 10.7 10.5 0.32
C18:3 8.4 8.2 8.3 7.7 0.41
CLA 18.4 17.6 19.9 16.7 1.87
a
Standard error of difference.
of Jiang et al. (1996). Trans-11-C18:1is formed as an centrations of C18:0 and C18:1 than the IH and DH intermediate during the biohydrogenation of dietary breeds.
linoleic to stearic acid (Kepler and Tove, 1967).
Acknowledgements 4. Conclusions
We thank Michael Pariza, Food Research Institute, The Montbeliardes tended to be higher producers University of Wisconsin, Madison, WI, USA for of milk fat CLA than the other breeds examined. The generously providing the purified CLA standard. The large variation between cows within each breed authors wish to thank Mr. P. O’Connor for taking the indicates that factors other than breed influence the milk samples. The technical assistance of Seamus CLA content of milk. There was a significant Aherne is gratefully acknowledged. This work was correlation between CLA levels of individual cows at supported by grants from the research levy con-the two sampling times. This indicates that, within tributed by Irish dairy farmers and by the European one lactating season cows producing high or low Union (Concerted Action FAIR-CT98-3671). milk fat CLA concentrations may continue to do so
throughout the season. This may indicate the
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