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© 2007 The American Society for Nutrition J. Nutr. 137:71-76, January 2007

Nutrient Physiology, Metabolism, and Nutrient-Nutrient Interactions

Trans-10 Octadecenoic Acid Does Not Reduce Milk Fat Synthesis in Dairy Cows1,2

Adam L. Lock3,6, Cynthia Tyburczy3, Debra A. Dwyer3, Kevin J. Harvatine3, Frédéric Destaillats4, Zéphirin Mouloungui5, Laure Candy5 and Dale E. Bauman3,*

3 Department of Animal Science, Cornell University, Ithaca, NY 14853; 4 Nestlé Research Center, Vers-chez-les-Blanc, Lausanne, Switzerland; and 5 Laboratoire de Chimie Agro-Industrielle UMR 1010, INRA/INP-ENSACIET, Toulouse, France

* To whom correspondence should be addressed: deb6{at}cornell.edu.


   ABSTRACT
TOP
 ABSTRACT
Introduction
 Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 
Diet-induced milk fat depression (MFD) involves the interrelation between rumen fermentation and mammary synthesis of milk fat, and the reduction in milk fat coincides with a marked increase in the trans-10 18:1 content of milk fat. Our objective was to directly examine the effect of trans-10 18:1 on milk fat synthesis in dairy cows. Three mid-lactation cows were used in a 3 x 3 Latin square design; treatments were abomasal infusion of: 1) ethanol (control); 2) trans-10 18:1 (t10); and 3) trans-10, cis-12 conjugated linoleic acid (CLA; positive control). The t10 and CLA supplements (>90% purity) were infused for 4 d and provided 42.6 and 4.3 g/d of trans-10 18:1 and trans-10, cis-12 CLA, respectively. Milk yield, feed intake, milk protein, and milk lactose were unaffected by treatment. Compared with the control, the t10 treatment had no effect on milk fat synthesis, whereas the CLA treatment resulted in a 27 and 24% reduction in milk fat content and yield, respectively. The transfer efficiency of the abomasally infused trans-10 18:1 and trans-10, cis-12 CLA into milk fat was 15 ± 1 and 23 ± 5% (means ± SD), respectively. Overall, trans-10 18:1 had no effect on milk fat synthesis when abomasally infused at ~43 g/d, although it was taken up by the mammary glands and incorporated into milk fat. Therefore, our results offer no support for the concept that changes in rumen production of trans-10 18:1 within the physiological range play a role in the regulation of fatty acid synthesis during diet-induced MFD.


   Introduction
TOP
 ABSTRACT
 Introduction
Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 
Fat, the most variable component in milk, is affected by many physiological and environmental factors (1,2). Nutrition is the predominant environmental factor and one of the most striking examples in ruminants is the low-fat milk syndrome, more commonly referred to as milk fat depression (MFD)7. Diet-induced MFD is a naturally occurring situation that involves an interrelation between rumen fermentation and mammary synthesis of milk fat (3). Davis and Brown (4) were among the first to recognize that diet-induced MFD coincided with a marked increase in the milk fat content of trans-18:1 fatty acids and subsequent research demonstrated this involved a dramatic shift in the trans-18:1 fatty acid profile (5). In ruminants, trans fatty acids are produced as intermediates in the biohydrogenation of dietary fatty acids; thus, diet-induced MFD coincides with an alteration in rumen biohydrogenation and the production of unique fatty acid intermediates.

The first rumen biohydrogenation intermediate shown to inhibit milk fat synthesis was trans-10, cis-12 conjugated linoleic acid (CLA; 6), but additional, as yet unidentified, inhibitory intermediates must exist (3,7). The trans-18:1 fatty acid that closely parallels MFD is trans-10 18:1 (3,8) and a summary of data from 35 publications involving 109 treatments demonstrated a curvilinear relation between an increase in milk fat content of trans-10 18:1 and a reduction in milk fat percent (R2 = 0.54; 9). Although some have concluded that trans-10 18:1 must cause MFD, correlated changes do not establish a cause-effect relation and the lack of trans-10 18:1 availability has precluded a direct examination of its effect on milk fat synthesis.

Our objective was to directly examine the effect of trans-10 18:1 on mammary synthesis of milk fat in dairy cows. Pure trans-10 18:1 was provided by abomasal infusion as a convenient experimental method to by-pass possible alterations within the rumen. We observed that trans-10 18:1 was taken up by the mammary gland and transferred to milk fat, but it had no effect on milk fat synthesis even when provided at a dose 10 times greater than the effective dose of trans-10, cis-12 CLA.


   Materials and Methods
TOP
 ABSTRACT
 Introduction
 Materials and Methods
Results
 Discussion
 LITERATURE CITED
 
    Cows and experimental design. All experimental procedures were approved by the Cornell University Institutional Animal Care and Use Committee. Three rumen fistulated mid-lactation cows (219 ± 37 d postpartum; mean ± SD) were randomly assigned in a 3 x 3 Latin square experiment. Treatments were abomasal infusion of: 1) ethanol (control); 2) trans-10 18:1 (t10 treatment); and 3) trans-10, cis-12 CLA (CLA treatment). The trans-10 18:1 (free fatty acid) and trans-10, cis-12 CLA (methyl ester) were solubilized in 95% ethanol at a ratio designed to maintain the same rate of ethanol infusion (180 mL/d). Treatments were infused into the abomasum via a 0.5-cm (i.d.) polyvinyl chloride tubing that passed through the rumen fistula and sulcus omasi (10). Solutions were prepared fresh daily and equal proportions infused every 6 h. Treatment periods were 4 d in duration followed by a 7-d washout period to minimize carryover effects in the next treatment period.

    Fatty acid supplements. We synthesized the trans-10 18:1 free fatty acid supplement (95% trans-10 18:1) and purified it according to previously described procedures (11–14). The supplement was a clear yellow solid melting at 52–53°C. The trans-10, cis-12 CLA methyl ester supplement (96% trans-10, cis-12 CLA) was provided by BASF AG. The fatty acid composition (Table 1) of both supplements was determined using GC conditions described previously (15). Additional analyses were carried out to confirm that trans-10 18:1 was the principle fatty acid present in the trans-10 18:1 supplement. The supplement was derivatized with trimethylsulfonium hydroxide (Macherey-Nagel) and analyzed by GC using a CP Select CB-FAME column (0.25-mm i.d., 0.25-µm film thickness, 50 m long, Varian). The oven was kept at 185°C for 40 min then ramped to 250°C at 15°C/min and finally held at 250°C for 10 min. Helium was used as carrier gas with a flow of 1.2 mL/min; injection volume was 1 µL. The temperatures of injector and flame ionization detector were both 250°C. The analysis revealed a purity level of 97% trans/3% cis composition in 10-octadecenoic acid. To confirm the geometry of the ethylenic double bond, infrared spectroscopy was performed using a FTIR 460 Plus spectrometer (JASCO) and 1H and 13C NMR spectra were recorded from a Bruker Advance apparatus at 500 MHz. Finally, the supplement was analyzed by NMR in CDCl3 (99%, Sigma-Aldrich).


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  		TABLE 1 Fatty acid composition of the supplements providing trans-10 18:1 and trans-10, cis-12 CLA1

 
    Sampling and analysis. Throughout the study, cows were housed in tie stalls at the Cornell University Large Animal Teaching and Research Unit and consumed ad libitum a total mixed ration formulated using the Cornell Net Carbohydrate and Protein System (16) to meet or exceed nutrient requirements (17). The diet was sampled during each experimental period and nutrient composition determined by wet chemistry procedures (Table 2; 18; Dairy One Cooperative). Cows were milked at 0700 and 1900 daily and samples obtained at each milking. One aliquot was stored with preservative (bronopol tablet; D&F Control System) at 4°C until analyzed for fat, true protein, lactose, and somatic cells using a mid-infrared spectrophotometer (18; Dairy One Cooperative). A second aliquot was stored without preservative at –20°C until analyzed for fatty acid composition. Milk lipids were subsequently extracted, transmethylated, and methyl esters quantified by GC according to Perfield et al. (15). On the final day of each treatment, period blood samples were taken from the coccygeal vein with sodium heparin (100 kU/L of blood) used to prevent coagulation. Plasma was harvested (2,300 x g; 15 min at 4°C) and stored at –20°C. Plasma lipids were subsequently extracted and methylated as described previously (19) and fatty acid composition determined (15).


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  		TABLE 2 Ingredient and nutrient composition of diet

 
    Statistical analyses. Data were analyzed as a 3 x 3 Latin square design using the fit model procedure of JMP (Version 5, SAS Institute). The model to test treatment means included the random effect of cow and fixed effect of period and treatment. Period was removed from the statistical model when declared nonsignificant at P > 0.20. Preplanned contrasts included the overall effect of treatment, the effect of trans-10 18:1 (t10 vs. control), and the effect of trans-10, cis-12 CLA (CLA vs. control). Effects were declared significant at P < 0.05.


   Results
TOP
 ABSTRACT
 Introduction
 Materials and Methods
 Results
Discussion
 LITERATURE CITED
 
    Choice of dose. To our knowledge, this study represents the first direct examination of the effect of trans-10 18:1 on milk fat synthesis in ruminants. Therefore, choosing an appropriate dose of trans-10 18:1 to adequately test our hypothesis was fundamental and this was especially critical given the limited availability of trans-10 18:1. The dose chosen was based on 2 lines of evidence and was designed, if inhibitory, to produce a significant reduction in milk fat yield. First, several studies have measured trans-10 18:1 outflow from the rumen (20–24) and a plot of these data in relation to milk fat content is shown in Figure 1. Across these 5 studies, it is apparent that rumen outflow of trans-10 18:1 increases during dietary situations where MFD occurs, and the reduction in milk fat percent is substantial when rumen outflow is over 30 g/d.


Figure 1
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  		Figure 1  Relationship between rumen outflow of trans-10 18:1 and milk fat content. All data were taken or calculated from experiments reported in 5 independent studies.

 
Our second line of evidence was based on studies in which abomasal infusions of partially hydrogenated vegetable oil (PHVO) have been shown to reduce milk fat secretion in dairy cows (25,26). PHVO typically contain a Gaussian distribution of trans fatty acids (40–50% of total fatty acids) with trans-9 18:1, trans-10 18:1, and trans-11 18:1 being the most prevalent (27). The aforementioned studies observed a 14 to 25% reduction in milk fat synthesis when PHVO was abomasally infused, and given the characteristic fatty acid composition of PHVO (27), they would have supplied ~40 to 60 g/d of trans-10 18:1. Therefore, based on the relation between daily duodenal flow of trans-10 18:1 and milk fat content and the available data from abomasal infusion studies with PHVO, we concluded that a dose of ~40 g/d would provide a sound test of any cause-effect within the range of trans-10 18:1 typically present in lactating dairy cows.

Trans-10, cis-12 CLA has been shown consistently to reduce milk fat yield in dairy cows. The dose chosen (~4 g/d) for this study was based on the dose-response relation previously generated from published studies (28) and was estimated to cause ~30% reduction in milk fat yield. This dose also represented only 10% of the dose chosen for trans-10 18:1.

    Performance responses to fatty acid infusions. The infusates provided 42.6 and 4.3 g/d of trans-10 18:1 and trans-10, cis-12 CLA in their respective treatments. The t10 and CLA treatments had no affect on feed intake (data not shown; mean = 20.2 kg/d) or milk yield (Table 3; mean = 29.1 kg/d). Likewise, milk protein and lactose yield and somatic cell count did not differ among treatments (data not shown).


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  		TABLE 3 Effect of trans-10 18:1 and trans-10, cis-12 CLA on milk yield and milk fat synthesis of lactating cows1

 
Compared with the control treatment, the t10 treatment had no effect on milk fat synthesis, whereas the CLA treatment resulted in a 27 and 24% reduction in milk fat content and yield, respectively (Table 3). The temporal pattern for milk fat content and yield demonstrated a progressive decline for cows receiving the CLA treatment with a return to previous values when the infusion was terminated (Fig. 2). The reduction in milk fat content and yield with the CLA treatment involved decreased secretion of both de novo and preformed fatty acids (Table 3). However, the decrease was greater for the short and medium chain fatty acids, resulting in a shift in milk fat composition to an increased proportion of long chain fatty acids (Supplemental Table 1).


Figure 2
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  		Figure 2  Temporal pattern of milk fat content (Panel A) and yield (Panel B) during abomasal infusion of trans-10 18:1 (t10) and trans-10, cis-12 CLA in lactating cows. Cows received supplements for 4 d (dotted lines). Values represent means from 3 cows; SEM = 0.09% and 0.06 kg/d, respectively.

 
    Incorporation of infused fatty acids. The temporal pattern for the incorporation of trans-10 18:1 and trans-10, cis-12 CLA into milk fat demonstrated a progressive increase following initiation of infusion and a plateau by d 3 of infusion (Fig. 3). During the control and CLA treatments, the trans-10 18:1 content of milk fat was not different and present at concentrations typically observed in dairy cows (~0.5 g/100 g fatty acids). During the t10 treatment period, the trans-10 18:1 content of milk fat increased steadily to 1.11 g/100 g of total fatty acids on d 4 of infusions. After correcting for endogenous levels in milk fat, the transfer efficiency of the abomasally infused trans-10 18:1 into milk fat was 15 ± 1% (mean ± SD). Milk fat content of trans-10, cis-12 CLA was undetectable (<0.01 g/100 g fatty acids) during the control and t10 treatment periods. However, during the CLA treatment period, the milk fat content of trans-10, cis-12 CLA increased to 0.13 g/100 g of total fatty acids on d 4 and this represented a transfer efficiency of 23 ± 5% (means ± SD).


Figure 3
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  		Figure 3  Temporal pattern of the incorporation of trans-10 18:1 (t10; Panel A) and trans-10, cis-12 CLA (Panel B) into milk fat of lactating cows. Data presented on a content basis (g/100 g fatty acids) from milk collected at each milking during the infusion period; infusions started after the zero (0) milking. Values represent means from 3 cows; SEM = 0.10 and 0.01 g/100 g for trans-10 18:1 and trans-10, cis-12 CLA, respectively. Trans-10, cis-12 CLA was undetectable (<0.01 g/100 g fatty acids) during both the control and t10 treatment periods.

 
The concentration of trans-10 18:1 in plasma lipids was increased on d 4 of the t10 treatment. Values were 0.16 and 0.36 g/100 g fatty acids for control and t10 treatments, respectively (P = 0.002; SEM = 0.03); control and CLA treatments did not differ (P = 0.39). Trans-10, cis-12 CLA in plasma lipids was undetectable (<0.01 g/100 g fatty acids) during the control and t10 treatment periods. Compared with the control treatment, the CLA treatment increased the plasma lipid concentration of trans-10, cis-12 CLA to 0.08 g/100 g fatty acids on d 4 of treatment (P < 0.001; SEM < 0.01).


   Discussion
TOP
 ABSTRACT
 Introduction
 Materials and Methods
 Results
 Discussion
LITERATURE CITED
 
Diet-induced MFD is a naturally occurring situation that involves an interrelation between rumen fermentation and mammary metabolism whereby alterations in the pathways of rumen biohydrogenation result in the production of fatty acid intermediates that inhibit fatty acid synthesis in the mammary gland (3). The established major pathway of rumen biohydrogenation involves the formation of trans-11 18:1 and cis-9, trans-11 CLA as intermediates in the biohydrogenation of linoleic acid (29). However, under certain dietary situations, a portion of unsaturated fatty acids undergo biohydrogenation via other pathways and some of these intermediates are known to be potent inhibitors of milk fat synthesis, the most extensively studied being trans-10, cis-12 CLA (6,28).

Rumen production of many biohydrogenation intermediates is increased when diets causing MFD are consumed by dairy cows and some of these are likely to be inhibitory for milk fat synthesis (3,7). One of particular interest is trans-10 18:1, which is an intermediate in the biohydrogenation pathway that produces trans-10, cis-12 CLA. Rumen outflow of trans-10 18:1 increases substantially during MFD (Fig. 1) and other investigations have demonstrated a curvilinear relation between the trans-10 18:1 increase in milk fat and the reduction in milk fat percent (8,9). However, correlated changes do not establish a causal relation and the increase in the rumen outflow of trans-10 18:1 and its subsequent incorporation into milk fat could simply be a marker for altered rumen biohydrogenation pathways rather than having an inhibitory effect per se. In this study, abomasal infusion of 43 g/d of trans-10 18:1 had no effect on the content or yield of milk fat. This contrasts with trans-10, cis-12 CLA where abomasal infusion of one-tenth this dose resulted in a milk fat reduction of ~25%.

In the current experiment, the 4-d infusion period was sufficient to give a plateau in the incorporation of trans-10 18:1 in milk fat, and by d 4, the milk fat content was 1.4-fold greater than control. This increase is comparable to the 1.3-fold increase in the trans-10 18:1 content of plasma lipid. The transfer efficiency of the abomasally infused trans-10 18:1 into milk fat was 15%, which is similar to the 17 ± 3% (mean ± SD) transfer efficiency recently reported for trans-10, trans-12 CLA (15). However, this transfer is lower than that observed for trans-10, cis-12 CLA in this study (23%) and the mean of 22% for 6 studies in which trans-10, cis-12 CLA was abomasally infused (28). Because there is no published literature examining the effects of trans-10 18:1, we are unable to ascertain whether the low transfer efficiency for trans-10 18:1 is a consequence of a low absorption from the small intestine or the fact that trans-10 18:1 is more extensively oxidized and used for processes other than milk fat synthesis. However, the available data indicate that the small intestine digestibility of trans-10 18:1 is not markedly different from the digestibility of other 18-carbon fatty acids (22,24).

Based on the changes in the trans-10 18:1 content of milk fat observed in this study and using the equation generated from the available data (35 publications involving 109 treatments; 9), the observed 0.64 g/100 g fatty acids increase in the trans-10 18:1 content of milk fat would predict a corresponding reduction in milk fat percentage of 0.32 units. However, our results show that despite the fact that trans-10 18:1 was absorbed, taken up by the mammary gland, and transferred to milk fat, it had no effect on milk fat synthesis. Whereas this study is the first, to our knowledge, to directly examine the effect of trans-10 18:1 on milk fat synthesis in ruminants, indirect support for our results comes from studies in which oleic acid supplements were fed to dairy cows (9,30,31). The rumen biohydrogenation of oleic acid (cis-9 18:1) results in the formation of a wide range of trans-18:1 fatty acids, including trans-10 18:1 (32), with the result that feeding oleic acid can increase the rumen outflow and incorporation of trans-18:1 fatty acids into milk fat. Feeding dairy cows high levels of oleic acid (31) or canola oil (78% oleic acid; 30) resulted in an ~1.5-fold increase in the trans-18:1 content of milk fat, but milk fat yield was unaltered; however, these studies did not determine the trans-18:1 isomer profile. A similar study using improved analytical techniques showed that a 3-fold increase in the milk fat content of trans-10 18:1 correlated with MFD when cows received a high linoleic acid supplement, but a similar magnitude of increase in trans-10 18:1 induced by supplementing oleic acid occurred with no MFD (9). Other trans-18:1 fatty acids that have been directly examined include trans-9, trans-11, and trans-12 18:1 and none affected milk fat yields at the doses tested (12.5–25 g/d; 33, 34). To our knowledge, there is only one other study that examined the effects of a relatively pure source of trans-10 18:1 on lipid metabolism; Park et al. (35) found that feeding trans-10 18:1 at 0.27% of the diet to mice had no effect on body fat.

As mentioned previously, dietary supplements or abomasal infusions of PHVO have been shown to cause a reduction in milk fat (25,26) and these are often cited as evidence that trans 18:1 fatty acids, particularly trans-10 18:1, is an inhibitor of milk fat synthesis. Furthermore, PHVO have also been implicated in reduced milk fat in other species, including humans (36), mice (37), and pigs (38). However, data from this study do not support the hypothesis that the trans-10 18:1 present in these PHVO supplements was responsible for the observed reduction in milk fat. A probable explanation for these disparate results relates to the diverse range of fatty acids that can be produced during the production of PHVO. In addition to trans-10, cis-12 CLA, recent work has identified cis-10, trans-12 CLA and trans-9, cis-11 CLA as additional biohydrogenation intermediates that are potent inhibitors of milk fat synthesis in dairy cows (39,40) and other investigators have established that conjugated diene 18:3, 20:5, and 22:6 fatty acid supplements reduce body fat accumulation in rodents (41–43). The chemical hydrogenation process used in the production of PHVO is typically optimized to produce trans 18:1 fatty acids, with trans-9, trans-10, and trans-11 the most prevalent (27). However, detailed analysis of PHVO has revealed that a range of trans and conjugated PUFA can also be produced during this process (44–46) and 1 or more of these fatty acids could play a role in the reduction in milk fat observed with PHVO.

In conclusion, whereas trans-10 18:1 was taken up by the mammary gland and transferred to milk fat, it had no effect on milk fat synthesis even when provided at a dose 10 times greater that the effective dose of trans-10, cis-12 CLA. Therefore, this study offers no support for trans-10 18:1 as a cause of diet-induced MFD and highlights the problem of implying cause-effect relations based on correlations between specific milk fatty acids and MFD.


   ACKNOWLEDGMENTS
 
The assistance of the following students and colleagues in implementing the study is gratefully acknowledged and appreciated: S. Stachnik, E. Johnson, B. Berggren-Thomas, A. O'Donnell, L. Furman, D. Parr, G. Birdsall, W. Jones, and B. Jones.


   FOOTNOTES
 
1 Supported by the National Research Initiative Competitive Grants Program, Cooperative State Research, Education, and Extension Service, USDA (grant no. 2006-35206-16643) and by the Cornell Agricultural Experiment Station. Back

2 Supplemental Table 1 is available with the online posting of this paper at jn.nutrition.org. Back

6 Present address: Department of Animal Science, University of Vermont, Burlington, VT 05405. Back

7 Abbreviations used: CLA, conjugated linoleic acid; MFD, milk fat depression; PHVO, partially hydrogenated vegetable oil. Back

Manuscript received 13 September 2006. Initial review completed 14 October 2006. Revision accepted 24 October 2006.


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 ABSTRACT
 Introduction
 Materials and Methods
 Results
 Discussion
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