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Dairy Science Department, South Dakota State University, Brookings, South Dakota 57007-0647
4To whom correspondence should be addressed: Dr. Sharon T. Franklin, Animal Science Department, University of Kentucky, 408 W.P. Garrigus Bldg., Lexington, KY, 40546-0215. Telephone: (606) 257-3248, Fax: (606) 257-7537, e-mail: sfrankli{at}ca.uky.edu
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONREFERENCES |
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KEY WORDS: • bovine • (n-3) fatty acids • conjugated linoleic acid • transvaccenic acid • dairy cattle
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONREFERENCES |
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) which have been implicated as a factor for increased risk
of heart disease (Ney 1991
). Also, long-chain (n-3)
fatty acids, which have been associated with a decrease in the risk of
heart disease (Albert et al. 1998
, Daviglus et al. 1997
), are lacking in milk fat. Many attempts have been
made, therefore, to alter the fatty acid composition of milk fat from
dairy cows to improve the nutritional value for consumers (Baer 1996
).
Researchers have attempted to increase unsaturated fatty acids in milk
fat through various modifications of diets of dairy cows
(Grummer 1991
). Early research (Brumby et al. 1972
, Pennington and Davis 1975
) investigated
the use of cod-liver oil as a nutritional supplement that had
potential for increasing unsaturated fats in milk fat. Fish oil,
however, was considered toxic to rumen microorganisms and caused a
decrease in percentage of milk fat. Studies also were conducted using
cod-liver oil treated with formaldehyde to protect the unsaturated
fatty acids from metabolism in the rumen (Storry et al. 1974
). The process allowed incorporation of unsaturated fatty
acids into milk fat of ruminants, but the use of formaldehyde was not
approved in the United States.
Interest in using dietary fish oil to modify milk fat has increased.
Hagemeister et al. (1988)
recently reported that
abomasal infusion of fish oil resulted in incorporation of
long-chain (n-3) fatty acids into milk fat. Ashes et al. (1992)
fed fish oil treated with formaldehyde to ruminants and
reported increased concentrations of eicosapentaenoic
acid6
[EPA, 20:5(n-3)] and docosahexaenoic acid [DHA, 22:6(n-3)] in serum
and tissues of steers and sheep. These studies illustrated that it was
possible to alter the fatty acid profile of milk and body fat when
long-chain (n-3) fatty acids reach the abomasum of ruminants.
The objective of this study was to increase the amount of (n-3) fatty acids, or their derivatives, in milk fat from dairy cows by feeding marine algae, a source of long chain (n-3) fatty acids, that were unprotected from rumen biohydrogenation or protected from rumen biohydrogenation.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONREFERENCES |
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Nine primiparous Brown Swiss and 21 multiparous Holsteins in mid
lactation (average days in milk = 145.4, range = 56 to 214)
were used to determine effects of feeding rations rich in (n-3) fatty
acids on milk production and milk fat composition. Cows (three Brown
Swiss and seven Holsteins per treatment) were assigned to a control
diet or a treatment diet supplemented with 910 g daily of marine
algae (Schizochytrium sp.; Omega Tech, Inc., Boulder, CO) that were
protected against rumen biohydrogenation (P-algae) or 910 g daily
of unprotected algae (U-algae) (Table 1
). The algae were protected against rumen biohydrogenation by coating the
algae with xylose (U.S. Patent 5,789,001; LignoTech USA, Rothschild,
WI). One Holstein cow was removed from the P-algae diet because of
a displaced abomasum and all data from that cow were excluded. Animal
care was according to the Guide for Care and Use of Agricultural
Animals in Agricultural Research and Teaching, and all animal
procedures were approved by the Institutional Animal Care and Use
Committee at South Dakota State University.
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Control and treatment diets (with algae included) were formulated to be
isonitrogenous at 17% crude protein (Table 1)
. Feed samples were
collected on d -14, 0, 14, 28 and 42 and composited. Samples of
P-algae, U-algae and feed were analyzed for determination of dry
matter, percentage of protein, ether extract, ash, Ca, P, and acid
detergent fiber (AOAC 1990
); vitamin E (Combs and Combs, Jr. 1985
); and neutral detergent fiber (Van Soest et al. 1991
).
The chemical composition of diets fed to dairy cows is presented in
Table 2.
Diets were similar for all variables measured with the exception of fat
percentage. The marine algae supplements increased the percentage of
fat in the treatment diets. The lipid content of the P-algae
supplement was 19.7% fat, and the lipid content of the U-algae
supplement was 25.7% fat. The algae protected from ruminal
biohydrogenation provided less fat compared to the U-algae because
of the amount of xylose added to the algae during the protection
process.
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Inclusion of marine algae in the diets increased the percentage of
14:0, 16:0, 16:1 and cis-18:1(n-7) in the P-algae and U-algae
diets and decreased the percentage of cis-18:1(n-9), 18:2(n-6) and
18:3(n-3). The fatty acids, 22:5(n-6) and 22:6(n-3), were undetectable
in the control diet but contributed 6.07% of the fat for the
P-algae diet and 7.50% of the fat for the U-algae diet.
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Cows were milked at ~0430 and 1530 h daily with milk weights
recorded electronically at each milking. Milk samples were obtained
each Monday during the evening milking and each Tuesday during the
morning milking for the duration of the trial. Milk samples were
composited by cow each week and analyzed by the mid-infrared
spectroscopic method (Multispec; Foss Food Technology Corp., Eden
Prairie, MN) for fat, protein, solids-not-fat, and lactose
(Association of Official Analytical Chemists 1990
).
Somatic cell counts were determined using a Fossomatic 90 (Multispec).
Aliquots of composited samples were stored at -20°C for analysis of
fatty acids by gas chromatography.
Body weights of cows were recorded for three consecutive days beginning
on d -15, -1 and 41. Body condition of cows (Wildman et al. 1982
) was evaluated by three individuals on d -15, -1, and
41.
Gas chromatography.
Milk samples were analyzed for individual fatty acids by gas
chromatography of butyl esters (Hippen 1996
). Individual
fatty acids were identified by comparison of gas chromatography peaks
with peaks of known standards (Nu-Chek Prep, Elysian, MN). Briefly, 0.5
mL of milk was placed into 16 x 150 test tubes with
Teflon-lined screw caps, followed by addition of 750 µL of
n-butanol. Samples were vortexed at low speed while slowly
adding 75 µL of acetyl chloride. Samples were gassed with N, capped
tightly and heated at 100°C for 1.5 h. After samples cooled to
room temperature, 5 mL of 6% K2CO3 and 1 mL of
hexane were added and the samples were vortexed for 30 s. Samples
were centrifuged (20 min at 2500 x g), and the bottom
layer was aspirated and discarded. The remaining layer was washed three
times (20 min at 2500 x g) with distilled, deionized
water. The upper layer was then removed and placed in injection vials
for analysis.
Fatty acid analysis of butyl esters was conducted using an HP 6890 gas chromatograph (Hewlett-Packard, Palo Alto, CA) with a Supelco 2560 fused silica capillary column (Supelco, Bellefonte, PA). The injection and detector temperatures were 230°C, and the split ratio was 100:1. Oven temperature was set at 60°C for 5 min. Temperature was then increased 3°C/min to 165°C and held for 10 min, then increased by 5°C/min to 220°C and held for 25 min.
Sensory evaluation.
Milk samples from cows fed control, P-algae and U-algae diets
were pasteurized at 65.5°C for 30 min (with occasional agitation),
rapidly cooled and stored at 4°C. Milks were evaluated
(Larmond 1977
) within 3 d after pasteurization by
12 faculty and student panelists between the ages of 22 to 56 y
from the Dairy Science Department, South Dakota State University,
Brookings, SD. All the faculty had experience in milk sensory
evaluation and scoring. The student panelists had completed a course in
sensory evaluation of dairy products. Composite milk samples from 10
cows fed the control diet, 9 cows fed the P-algae diet, and 10 cows
fed the U-algae diet for each sample time (d -14, 0, 28 and 42)
were evaluated by the triangle test (Roessler et al. 1978
), a sensory evaluation procedure that will indicate if
detectable differences exist between samples. Two identical samples and
one odd sample comprised each set of samples tasted by panelists.
Panelists were asked to select the odd sample from each set, determine
the degree of difference between duplicate samples, and indicate any
possible off-flavors in the milk samples.
Statistical analysis.
Data were analyzed with the mixed model procedure of SAS (SAS 1996
) using repeated measures and appropriate covariates. Data
from the period just prior to moving cows to the Calan feeders were
used as covariates for milk production parameters. The means of body
weights taken on d -15, -14, and -13 were used as covariates for
body weights, and the body condition scores obtained on d -15 were
used as the covariates for body condition scores. Feed intake data
obtained during wk -2 were used as the covariates for feed intake.
Data are presented as covariate adjusted least squares means (LSM)
± SEM when the covariate was significant and as LSM
± SEM when the covariate was not significant.
Differences among LSM were determined using the predicted difference
option of the mixed model procedure of SAS. Week, breed and treatment
were tested as main effects. Differences were considered significant at
P < 0.05.
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONREFERENCES |
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). The Brown Swiss cows ate less (P < 0.05) dry matter
(15.6 kg/d) compared to the Holstein cows (21.9 kg/d); however, there
was no interaction (P > 0.05) between breed and
treatment, indicating the two breeds responded similarly to treatments.
Addition of fat as safflower seeds to diets of dairy cows has been
shown to decrease dry matter intake (Stegeman et al. 1992
). Other studies (Kim et al. 1991
and
Kim et al. 1993
, Schingoethe et al. 1996
) have shown no effect of feeding various fats on dry
matter intake. Supplementation of fish oil at 200 to 400 g/d to dairy
cows also resulted in decreased dry matter intakes in most studies
(Cant et al. 1997
, Doreau and Chilliard 1997
, Wonsil et al. 1994
). Spain et al. (1995)
reported no effect of feeding fish oil or ruminal
infusion of fish oil on dry matter intake; however, amounts
supplemented (~44 g) were lower than other studies. No other studies
have reported feeding marine algae to dairy cows. Whether the decrease
in intake was because of decreased palatability of the algae diets,
greater fat intake, or intake of particular fatty acids is unknown;
however, total fat content of diets was not dramatically different.
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)
was affected (P > 0.05) by feeding marine algae;
however, percentage and yield of fat from cows fed algae were lower
(P < 0.05) than in cows fed the control diet (Table 4)
. The Brown Swiss cows tended (P = 0.06) to produce
less energy-corrected milk compared to the Holstein cows; however,
there was no interaction between breed and treatment. These results are
similar to studies which fed unprotected fish oil (Brumby et al. 1972
, Cant et al. 1997
, Wonsil et al. 1994
) and also reported no effect on milk production but
reported decreased percentage and yield of milk fat. Feeding
cod-liver oil that was protected against ruminal metabolism by
formaldehyde treatment did not affect proportion and yield of milk fat
(Storry et al. 1974
).
Percentage of protein in milk from cows fed algae also tended
(P = 0.08) to be lower compared with percentage of
protein in milk from cows fed the control diet; however, protein yield
was not affected (P = 0.53) by diets (Table 4)
.
Body weights and body condition scores of cows were not affected
(P > 0.05) by feeding diets containing algae even
though milk production remained constant while dry matter intake
decreased (Table 4)
. Cows were fed algae for only 7 wk; thus, effects
of long-term feeding of algae on body condition and body weights
are not known. Because intake was lower without a decrease in
production, efficiency of production (energy-corrected milk/dry matter
intake) tended (P = 0.10) to be greater for cows fed
algae compared to cows fed the control diet.
Although production of milk by dairy cows fed algae was not greatly
affected, the fatty acid profile of milk fat from cows fed marine algae
was dramatically altered compared with milk fat from cows fed the
control diet (Table 5
). In general, feeding marine algae affected the fatty acid profile of the
milk fat from Brown Swiss and Holstein cows similarly. Total saturated
fatty acids were lower (P < 0.05) in milk fat from
cows fed marine algae compared to milk fat from cows fed the control
diet. Total unsaturated fatty acids were greater (P < 0.05) in milk fat from cows fed P-algae compared to cows fed the
control diet and tended (P = 0.09) to be greater in
milk fat from cows fed U-algae. The alteration in the proportions
of saturated fatty acids was mainly a result of lower (P
< 0.05) 18:0 and greater (P < 0.05)
polyunsaturated fatty acids, specifically DHA and conjugated linoleic
acid (CLA), in milk fat from cows fed algae. Concentrations of 14:0 and
16:0 were greater (P < 0.05) as well. Scientists
involved in a roundtable discussion (Berner 1993
) of the
role of milk fat in human diets agreed that saturated fatty acid intake
should be decreased. There was discussion, however, regarding effects
of specific saturated fatty acids on health of consumers. Some
saturated fatty acids are considered to be cholesterol-raising
(12:0, 14:0 and 16:0), whereas most fatty acids in milk fat are not. It
is unknown whether decreasing the proportion of total saturated fatty
acids while increasing total unsaturated fatty acids will improve the
cholesterol status of consumers if proportions of 14:0 and 16:0 are
also increased.
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. The proportion
of DHA also was greater (P < 0.05) in milk fat of cows
fed P-algae compared to milk fat from cows fed U-algae. Cows
fed P-algae consumed an average of 29.6 g of DHA daily and
secreted an average of 4.94 g of DHA in milk daily, for an average
transfer efficiency of 16.7%. Cows fed U-algae consumed an average
of 37.6 g of DHA daily and secreted an average of 3.17 g of
DHA in milk daily, for an average transfer efficiency of 8.4%. Thus,
the protection process used to produce P-algae prevented ruminal
biohydrogenation of DHA to an extent and allowed for more efficient
(P < 0.05) incorporation of DHA into milk fat. Over
the duration of the study, the proportion of DHA in milk fat of cows
fed P-algae was greatest (P < 0.05) on d 14,
decreased slightly (P < 0.05) by d 28, then remained
constant. The proportion of DHA in milk fat of cows fed U-algae
decreased (P < 0.05) gradually from d 14 to d 42
(Fig. 1A
). Rumen microorganisms may have become acclimated to the presence of
U-algae in the diet over time, resulting in greater
biohydrogenation of DHA with less incorporation of DHA into milk fat.
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). Based on the
amount of DHA incorporated in milk fat by cows fed P-algae,
consumers could double their intake of long-chain (n-3) fatty acids
by consuming dairy products equivalent to 710 mL of milk from cows fed
diets containing P-algae. Although 22:5(n-6) was present in algae, amounts of 22:5(n-6) in milk of cows fed algae were barely detectable and were not quantified. Reasons for uptake of DHA, but not 22:5(n-6), by the mammary gland are not known.
Total 18:1 fatty acids in milk fat did not differ among treatment
groups; however, proportions of individual 18:1 isomers in milk fat
were affected (P < 0.05) by diet (Table 5)
. Oleic
acid, cis-18:1(n-9) was lower (P < 0.05) by ~40%
whereas transvaccenic acid [TVA, trans-18:1(n-7)] was greater
(P < 0.05) by almost fivefold, from ~1.2% to an
average of 7.1%, in milk fat from cows fed algae compared with milk
fat from cows fed the control diet. The concentration of TVA in milk
fat of cows fed P-algae was greatest at 14 d, averaging
greater than 8%, then decreased (P < 0.05) through
the end of the study (Fig. 1B)
. The concentration of TVA in milk fat of
cows fed U-algae had decreased (P < 0.01) by d 42.
Other 18:1 isomers, cis- and trans-18:1(n-12), trans-18:1(n-9) and cis-18:1(n-7), were also greater (P < 0.05) in milk fat of cows fed algae. The increase in cis-18:1(n-7) is likely because of the increased amount of cis-18:1(n-7) in the diets containing algae. Reasons for the alterations in the other 18:1 fatty acid isomers are unknown.
Wonsil et al. (1994)
reported increased concentrations
of TVA in milk fat with decreased milk fat percentage from cows fed
fish oil. The authors speculated that the increase in TVA was a result
of incomplete ruminal biohydrogenation of unsaturated fatty acids from
the fish oil but could not determine the mechanism. One possibility was
that fish oil was toxic to bacteria involved in biohydrogenation. That
explanation is less likely for the present study because the algae is
in a granular form, therefore, the lipid is not fed as a free oil.
Kepler et al. (1966)
reported that TVA was a result of
incomplete biohydrogenation of 18:2 fatty acids from diets containing
fats; however, the amount of 18:2 supplied by the algae diets was lower
than the amount of 18:2 supplied by the control diet. Additionally, dry
matter intake was lower for cows consuming algae diets compared to cows
consuming the control diet; thus, the amount of 18:2 supplied to the
rumen by the algae diets was less than the 18:2 supplied to the rumen
by the control diet. The algae diets supplied 22:5(n-6) and 22:6(n-3)
which were lacking in the control diet. Mechanisms by which 22:5(n-6)
and 22:6(n-3) may alter fatty acid metabolism in the rumen to increase
TVA in milk fat have not been reported.
The concentration of CLA in milk fat was greater (P < 0.05) from cows fed marine algae compared to cows fed the control diet
(Table 5)
. Mean concentrations of CLA in milk fat did not differ
between cows fed P-algae or U-algae. Over time, however, the
concentration of CLA in milk fat of cows fed P-algae was greatest
at 14 d and decreased (P < 0.05) by 28 d;
whereas the concentration of CLA in milk fat of cows fed U-algae
remained constant through 28 d but decreased (P < 0.05) by 42 d (Fig. 1C)
. Less protection of 22:6(n-3) from
U-algae compared to P-algae may allow for the concentration of
CLA in milk fat being maintained at high levels for a longer period of
time.
CLA are a group of isomers that have been shown to inhibit cancer in
laboratory animals (Ha et al. 1990
, Ip et al. 1991
, Ip et al. 1994
, and
Ip et al. 1996
, Ip and Scimeca 1997
, Pariza and Hargraves 1985
, Thompson et al. 1997
). Knekt et al. (1996)
reported an
inverse relationship existed between milk consumption and breast cancer
in a study of Finnish women. The authors suggested that a component of
milk, possibly CLA, might help protect against breast cancer,
therefore; increased concentrations of CLA in milk fat may be
beneficial for consumers. Griinari et al. (1998)
reported increased concentrations of CLA in milk fat, from ~0.3% to
~2%, as a result of feeding corn oil. The amount of CLA in milk fat
can also be increased by pasture feeding (Precht and Molkentin 1997
). Milk fat from cows consuming pasture contained a mean of
0.87% CLA compared to 0.46% CLA in milk fat from cows fed hay, silage
and concentrate.
The mechanism for increased concentrations of CLA in milk fat of cows
fed diets rich in DHA, but low in linoleic acid, is unknown. CLA in
milk fat has been reported to be produced from linoleic acid by the
rumen bacterium, Butyrivibrio fibrisolvens, with CLA and TVA
as intermediates in the conversion of linoleic acid to stearic acid
(Kepler et al. 1966
). Trans fatty acids can
also be substrates for production of CLA in humans (Salminen et al. 1998
). Milk fat from cows fed diets rich in (n-3) fatty
acids may increase availability of CLA to humans both by increased
concentrations of CLA in dairy products and by increased concentrations
of TVA, a possible additional source of CLA, in dairy products. Studies
regarding the effects of feeding dairy products containing high
concentrations of both CLA and TVA on cancer are needed.
There were no flavor differences (P > 0.05) between
milk from cows fed P-algae vs. milk from cows fed the control diet
or between milk from cows fed U-algae vs. milk from cows fed the
control diet at d -14 (Table 6
). The mean of all data from d 0, 28 and 42 for milk from cows fed the
control diet vs. milk from cows fed the P-algae diet (13 panelists
correctly identified the odd milk sample out of 33 sets of milk)
indicated no difference (P = 0.72) in flavor.
Similarly, the mean of d 0, 28 and 42 for milk from cows fed the
control diet vs. milk from cows fed the U-algae diet (12 panelists
correctly identified the odd milk sample out of 33 sets of milk)
indicated no difference (P = 0.58) in flavor. Overall,
no flavor differences were observed among milks during any of the
treatment periods. Off-flavors such as oxidized flavor were not
reported in any of the milks. The milk from cows fed the control diet
developed a cooked flavor while milk from cows fed the algae diets did
not. Milk from cows fed algae had a slight feed-like flavor;
however the flavor was not objectionable. These flavors are given good
scores in a sensory evaluation and are not undesirable unless the
flavors are excessive.
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Feeding marine algae to cows resulted in production of milk containing improved fatty acid profiles with acceptable flavor. Milk yield was not affected by treatment; however, percentage and yield of milk fat were decreased by feeding algae. Production of milk with increased concentrations of CLA, TVA and DHA could have a significant impact on health of consumers.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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2 Supported in part by USDA Strengthening Grant #940417, National Science Foundation Grant OSR-9452894, and the South Dakota Future Fund.
3 Published with approval of the director of the South Dakota Agricultural Experiment Station as Publication Number 3104 of the Journal Series.
5 Current address: Animal Science Department, University of Kentucky, Lexington, KY 40546-0215.
6 Abbreviations used: CLA, conjugated linoleic acid; DHA, docosahexaenoic acid, 22:6(n-3); EPA, eicosapentaenoic acid,
20:5(n-3); LSM, least square means; P-algae, protected algae; TVA, transvaccenic acid, trans-18:1(n-7); U-algae, unprotected algae.
Manuscript received May 3, 1999. Initial review completed June 11, 1999. Revision accepted August 6, 1999.
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONREFERENCES |
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