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Responses to Increasing Amounts of High-Oleic Sunflower Fatty Acids Infused into the Abomasum of Lactating Dairy Cows¹

J. K. Drackley^*,2, T. R. Overton^*,3, G. Ortiz-Gonzalez^,4, A. D. Beaulieu^*,5, D. M. Barbano, J. M. Lynch and E. G. Perkins^,6

^* Department of Animal Sciences, and
Department of Food Science and Human Nutrition, University of Illinois, Urbana 61801
Department of Food Science, Cornell University, Ithaca, NY 14853

² Corresponding author: drackley{at}uiuc.edu

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS ACKNOWLEDGEMENTS REFERENCES

 
Increasing the oleic acid (18:1 cis-9) content of milk fat might be desirable to meet consumer concerns about dietary healthfulness and for certain manufacturing applications. The extent to which milk fat could be enriched with oleic acid is not known. Increasing the intestinal supply of polyunsaturated fatty acids decreases dry matter intake (DMI) in cows, but the effects of oleic acid have not been quantified. In a crossover design, 4 multiparous Holstein cows were abomasally infused with increasing amounts (0, 250, 500, 750, or 1,000 g/d) of free fatty acids from high-oleic sunflower oil (HOSFA) or with carrier alone. Continuous infusions (20 to 22 h/d) were for 7 d at each amount. Infusions were homogenates of HOSFA with 240 g/d of meat solubles and 11.2 g/d of Tween 80; controls received carrier only. The HOSFA contained (by wt) 2.4% 16:0, 1.8% 18:0, 91.4% 18:1 cis-9, and 2.4% 18:2. The DMI decreased linearly (range 22.0 to 5.8 kg/d) as the infused amount of HOSFA increased. Apparent total tract digestibilities of dry matter, organic matter, neutral detergent fiber, and energy decreased as the infusion increased to 750 g/d and then increased when 1,000 g/d was infused. Digestibility of total fatty acids increased linearly as infused fatty acids increased. Yields of milk, fat, true protein, casein, and total solids decreased quadratically as infused amounts increased; decreases were greatest when 750 or 1,000 g/d of HOSFA were infused. Concentrations of fat and total solids increased at the higher amounts of HOSFA. The volume mean diameter of milk fat droplets and the diameter below which 90% of the volume of milk fat is contained both increased as HOSFA infusion increased. Concentrations of short-chain fatty acids, 12:0, 14:0, and 16:0 in milk fat decreased linearly as HOSFA increased. The concentration of 18:1 cis-9 (19.4 to 57.4% of total fatty acids) increased linearly as HOSFA infusion increased. Concentrations of 18:1 cis-9 in blood triglyceride-rich lipoproteins increased linearly as infusion increased, whereas contents of 14:0, 16:0, 18:0, total 18:1 trans, and 18:2n-6 decreased linearly. The composition and physical characteristics of milk fat can be altered markedly by an increased intestinal supply of 18:1 cis-9, which could influence processing characteristics and the healthfulness of milk fat. However, an increased supply of free 18:1 cis-9 to the intestine decreased DMI and milk production.

Key Words: milk fat • oleic acid • fatty acid • supplemental fat

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS ACKNOWLEDGEMENTS REFERENCES

 
Increasing oleic acid in milk fat at the expense of medium-chain saturated fatty acids (FA) such as myristic acid and palmitic acid might be a desirable outcome for some applications. Myristic and palmitic acids have been implicated as causing unfavorable blood lipid changes in humans and thus increasing risk for coronary disease, whereas oleic acid is neutral or beneficial (Woodside and Kromhout, 2005). Increased oleic acid in milk fat may improve the characteristics of some dairy products; for example, increasing the oleic acid content improves the spreadability of butter at refrigerator temperature (Enjalbert et al., 1997, 2000). Previous research has demonstrated that it is feasible to increase oleic acid in milk fat by infusion of high-oleic acid oil into the abomasum (Christensen et al., 1994; LaCount et al., 1994; Bremmer et al., 1998) or duodenum (Chilliard et al., 1991; Enjalbert et al., 2000) and by supplementing long-chain fatty acids (LCFA) as calcium soaps or amides to increase the amount of oleic acid that escapes biohydrogenation in the rumen (Ashes et al., 1992; Lin et al., 1996; Jenkins, 1998). Oleic acid content in milk fat also can be increased by supplemental fats that undergo biohydrogenation in the rumen and increase intestinal supply of stearic acid, a portion of which is then desaturated to oleic acid in the gut or mammary gland (Enjalbert et al., 1997).

The maximum extent to which milk fat can be enriched with oleic acid and the resulting effects on other characteristics of milk, milk fat, and processing qualities are not known. Earlier research from our laboratory showed that oleic acid enrichment of milk fat increased linearly to 30.4% of total milk FA as the amount of FFA from high-oleic sunflower oil (HOSFA) infused into the abomasum increased from 0 to 400 g/d (LaCount et al., 1994). Supplemental oleamide at 3.5% of dietary DM increased oleic acid to 48% of total milk FA (Jenkins, 1998). In a second study, Jenkins (1999) fed increasing amounts of oleamide (to 5% of total dietary DM) and reached a maximum enrichment of 43.4% oleic acid in milk fat. We are unaware of dose-response studies that have attempted to achieve a greater postruminal oleic acid supply and enrichment in milk fat.

Practical technologies to substantially increase oleic acid escape from the rumen and delivery to the small intestine for absorption might have negative effects on DMI by cows. Diets supplemented with more unsaturated LCFA supplements decreased DMI more than did supplements consisting of mostly saturated FFA (Harvatine and Allen, 2005). Previously, we have shown that mixtures of unsaturated FFA infused into the abomasum depress DMI (Drackley et al., 1992; Christensen et al., 1994; Bremmer et al., 1998). Suppressive effects of postruminal soy LCFA on DMI were more than 2 times larger when the LCFA were supplied as FFA rather than as triglycerides (TG; Litherland et al., 2005), which explains the larger decreases in DMI in our experiments in which FFA were infused compared with experiments by others who infused intact TG (Gagliostro and Chilliard, 1991; Benson et al., 2001). Whether the negative effect of unsaturated LCFA on intake is attributable to specific LCFA has not been determined accurately. A mixture of FFA resembling the profile of palm oil, containing 37% oleic acid, had less effect on DMI than mixtures high in linoleic acid, but interpretation of the effects of oleic acid were confounded by the presence of appreciable quantities of trans-monoenes in the mixture (Bremmer et al., 1998). Therefore, the effects of oleic acid per se remain unclear.

Our hypothesis was that oleic acid reaching the small intestine would increase oleic acid in milk fat and decrease DMI in a dose-dependent manner. The objectives of this experiment were to determine the effects of increasing amounts of free oleic acid infused into the abomasum on DMI, total tract digestibility of nutrient fractions, milk yield and composition, and FA profiles in milk fat and blood TG.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS ACKNOWLEDGEMENTS REFERENCES

 
All procedures were conducted under protocols approved by the University of Illinois Laboratory Animal Care Advisory Committee. Four multiparous Holstein cows (mean DIM = 116) that had been fitted previously with ruminal cannulas (10-cm center diameter; Bar Diamond, Parma, ID) were housed in tie stalls fitted with rubber mats, were bedded with straw, and had continuous access to water from individual drinking cups. Cows were milked at 0630 and 1700 h and were allowed to exercise in an outside lot from 0700 to 0900 h daily. The lactation diet (Table 1) was mixed as a TMR and fed twice daily at the time of milking in amounts to ensure ad libitum intake. Orts were removed and weighed once daily.

The design of the experiment (Table 2) was essentially as used previously (LaCount et al., 1994; Graves et al., 2007). The 4 cows were administered the 2 treatments in a crossover design. After a 1-wk preliminary period in which cows were infused only with water, 2 cows received the control infusate and 2 cows received the HOSFA infusate. During this 5-wk experimental period (period 1), the 2 cows receiving the HOSFA infusate received each amount (0, 250, 500, 750, and 1,000 g/d) sequentially, with each amount being infused for 7 d before increasing to the next amount. During period 1, the 2 control cows received only the carrier infusate for the entire 5 wk. Measurements were made during the last 3 d of each infusion amount. At the end of wk 5, all cows were returned to water infusion for a 2-wk washout period before being changed to the opposite treatment for period 2. In period 2, the procedures were repeated so that the other 2 cows received the HOSFA doses in sequentially increasing amounts, and the cows that previously received HOSFA received the control infusate.

Milk was sampled from the last 6 milkings of each infusion period and stored on ice in a refrigerator until completion of the period. The samples were then composited on a daily basis according to daily milk production. Samples were composited cold after gentle inversion and pouring between containers. If fat adhered to the bottle, the bottle was swirled gently in warm water to loosen fat. Care was taken to avoid heating the samples to avoid alterations of milk fat globule size that occur upon reheating (Smith et al., 1995). An aliquot of the composite sample was used to determine the TS content in duplicate gravimetrically (AOAC, 2000; methods 33.2.26, 989.05). Another aliquot was shipped on ice by overnight courier to the Department of Food Science, Cornell University (Ithaca, NY). The milk was tested in duplicate for fat by Mojonnier ether extraction (AOAC, 2000; methods 33.2.26, 989.05). Kjeldahl N analysis was used to determine (in duplicate) CP N (AOAC, 2000; methods 33.2.11, 991.20), non-CN N (AOAC, 2000; methods 33.2.64, 998.05), and NPN (AOAC, 2000; methods 33.2.12, 991.21). All Kjeldahl N results were expressed on a protein basis (N x 6.38). True protein was calculated as the difference between CP and NPN (x 6.38), and CN was calculated as the difference between CP and non-CN N (x 6.38). Milk fat globule size distribution was determined by using a laser light-scattering particle size analyzer (Mastersizer E, Malvern Instruments, Worcester, UK) capable of determining particle size distribution between 1 and 80 µm, as described by Smith et al. (1995). A reverse Fourier optical lens with a 45-mm focal length was used, and only forward light scattering was measured. Casein micelles exert minimal influence on light scattering when only forward light scattering is used to measure the particle size distribution of milk fat globules. Two parameters were used to describe milk fat globule size distribution: d(4,3), the volume mean diameter (VMD), and d(0.9), the mean fat globule diameter below which 90% of fat volume is contained.

Milk FA were determined by GC analysis of butyl ester derivatives (prepared by methods 963.22, 42.1.29; AOAC, 2000) on a DB-WAX column (30 m x 0.25 mm x 0.25 µm; J & W Scientific, Folsom, CA). The gas chromatograph (model 6890, Hewlett-Packard, Avondale, CA) was equipped with a flame-ionization detector. Chromatographic conditions included a 50:1 split, with He as the carrier gas at 80 kPa gauge and a flow of 25 cm/s at 40°C. Column temperature was 45°C for 2 min, ramped to 230°C at 5°C/min, and then held constant at 230°C for 10 min. A reference standard (GLC-85, Nu Chek Prep Inc., Elysian, MN) was used for peak identification, and triheptadecanoin was used as an internal standard (10 mg/mL; Nu Chek Prep).

Samples of the TMR were obtained on the last 4 d of each sampling week and were frozen at –20°C. At the end of each sampling week, the individual samples were dried at 55°C in an oven for determination of DM content. Samples then were ground through a 2-mm screen in a Wiley mill (Arthur H. Thomas, Philadelphia, PA), composited on an equal-weight basis, re-ground through a 1-mm screen, and stored in glass bottles until analyzed. Orts from individual cows on days that feed samples were obtained were sampled, dried, and ground as described for TMR samples. The dried and ground samples were composited in proportion to the amount of orts DM each day. Cows were dosed continuously with chromic oxide (10 g in gelatin capsules) twice daily at 0900 and 2100 h via the ruminal cannula. Fecal grab samples were collected at the time of chromium dosing on the last 4 d of each sampling week. Samples were composited immediately by placing 150-g subsamples in a covered plastic pan stored at –20°C. After the last sample was collected, the pan was dried in an oven at 55°C. Dried samples were ground through a 1-mm screen.

Samples of TMR, orts, and feces were analyzed for contents of DM (loss of weight after drying at 105°C), ash (600°C for 8 h), CP by Kjeldahl (method 984.13; AOAC, 2000), NDF using -amylase (Van Soest et al., 1991), ADF (Van Soest et al., 1991), total FA (Sukhija and Palmquist, 1988), and gross energy by bomb calorimetry (1261 Isoperibol Calorimeter, Parr Instrument Co., Moline, IL). Chromium content of feces was analyzed by atomic absorption spectrophotometry (Williams et al., 1962) to calculate apparent digestibilities of nutrient fractions in the total tract.

Blood was sampled by jugular venipuncture on d 6 of each period 3 h after the a.m. feeding for determination of the FA profile of TG in TG-rich lipoproteins. Procedures for collection of blood, separation of TG-rich lipoproteins by centrifugation, extraction of lipids, methylation of FA, and GC analysis were as described by Beaulieu et al. (2002). An additional blood sample was collected before the a.m. feeding on d 5. The evacuated tubes containing sodium heparin (Vacutainer, Becton Dickinson Vacutainer Systems USA, Rutherford, NJ) were centrifuged to obtain plasma, which was stored at –20°C until analyzed for concentrations of NEFA (Johnson and Peters, 1993) and glucose by glucose oxidase (kit number 315, Sigma Chemical Co.; Trinder, 1969).

Data were analyzed statistically by using PROC MIXED of SAS (version 9.1, SAS Institute Inc., Cary, NC). The model contained the random effect of cow and fixed effects of period (i.e., the 5-wk sets of infusion amounts within each treatment type; 1 df), treatment (control or HOSFA; 1 df), amount infused (as a subplot; 4 df), and the interaction of treatment and amount (4 df). Because of concerns about how cows would tolerate sudden and large changes in amounts of HOSFA infused, infusion amounts could not be randomized within periods 1 and 2 and were thus administered sequentially. Therefore, by design, the effect of amount was confounded with time (i.e., weeks). In this analysis, the statistical parameter of interest is the interaction of treatment by amount (LaCount et al., 1994; Graves et al., 2007), which here determined whether cows receiving the HOSFA treatment responded differently with advancing amount (i.e., weeks) compared with control cows. We anticipated that measurements for control cows would be essentially constant over each 5-wk infusion period. The effects of amount and the interaction of treatment by amount were tested by using the error term of cow nested within period and treatment. To model the effects of amount and its interaction with treatment, the REPEATED statement within PROC MIXED of SAS was used. The within-subjects variation was examined by using several covariance structures, and the one yielding the lowest Akaike’s information criterion was used in the analysis (Littell et al., 1998, 2000). For all variables, this was the AR(1) option. Polynomial contrasts were constructed to partition the treatment by amount interaction into single degree of freedom interactions of the linear, quadratic, and cubic effects of amount by treatment, and the P-values associated with these contrasts are tabulated. Degrees of freedom were determined by using the Kenward-Roger method (Littell et al., 1996). Model residuals were examined and for all variables were normally distributed. Least squares means were calculated and are presented with their standard errors throughout. Significance was declared at P < 0.05.

	RESULTS AND DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS ACKNOWLEDGEMENTS REFERENCES

 
Actual amounts of LCFA infused (Table 3) were slightly less than target values because of small amounts of the HOSFA adhering to the sides of the container and variations in pump flow rate. For the 1,000 g/d infusion, 2 cows stopped eating and milk yield dropped to less than 4 kg/d within 2 d of infusion at that amount; consequently, infusion of the 2 cows was terminated and data were not included for this amount. Actual LCFA infused for the 2 cows at the 1,000 g/d target dosage was 856 g/d. Cows returned to preinfusion milk and DMI within 10 d after the infusion ended. Because we allowed a 14-d washout period between infusion types, we are confident that carryover effects were minimal and did not confound our results. Cows also have returned to preinfusion values within 7 d after abomasal LCFA infusions ceased in our previous experiments (Drackley et al., 1992; Christensen et al., 1994; LaCount et al., 1994; Bremmer et al., 1998; Litherland et al., 2005). Infusion of HOSFA did not cause diarrhea at any infusion amount. In contrast, abomasal infusion of more than 450 g/d of soy FFA (containing large amounts of 18:2 and 18:3) resulted in diarrhea in an earlier experiment (Drackley et al., 1992).

Apparent total tract digestibilities of DM, OM, NDF, and energy (Table 4) were affected by interactions of treatment with the cubic effects of increasing infusion amount. Digestibilities for these fractions trended downward as HOSFA infusion increased to 750 g/d, and then increased sharply when 1,000 g/d was infused. Measurements made at the highest infusion amount may be less accurate because data were available for only 2 cows and DMI and fecal output were very low. In contrast, digestibility of total LCFA increased linearly as infusion increased. These data confirm the high intestinal digestibility of oleic acid reaching the small intestine in dairy cows (Klusmeyer and Clark, 1991; Enjalbert et al., 1997; Jenkins, 1998, 1999). Amounts of oleic acid delivered and absorbed postruminally were substantially greater than observed under typical dietary scenarios.

Changes in milk fat composition (Table 6) generally were as predicted based on established knowledge of factors affecting FA composition when cows are fed diets supplemented with fats and oils (Palmquist et al., 1993). Increasing the amount of HOSFA infused into the abomasum tended (P < 0.06) to linearly decrease the concentration of 4:0. Increasing HOSFA resulted in significant linear decreases in percentages of 6:0, 8:0, 10:0, 12:0, 14:0, 14:1, 15:0, 16:0, 18:0, and 18:3n-3 (Table 6). The content of 18:1 cis-9 increased linearly as infusion increased, whereas the percentages of 16:1 cis-7, 18:1 trans, and 18:2n-6 were not affected.

The changes in milk fat composition resulting from increased supply of oleic acid to mammary cells likely occurred through decreased de novo synthesis of short-and medium-chain FA (Palmquist et al., 1993) as well as mass-action effects on esterification from the increased supply of oleic acid relative to other FA. Oleic acid is found in milk TG at all 3 sn-positions of glycerol. Breckenridge and Kuksis (1968) reported that distribution of oleic acid was in a ratio of approximately 3:1.8:1 for the sn-1, sn-2, and sn-3 positions, respectively. Esterification of oleic acid at the sn-1 site would predominantly displace 14:0, 16:0, and 18:0, whereas oleic would primarily displace 14:0 and 16:0 at the sn-2 position (Breckenridge and Kuksis, 1968). The short-chain FA 4:0 and 6:0 are found almost exclusively at the sn-3 position, which likely explains the marked decrease of these FA by the increased oleic acid supply in our study.

Manufacturing and organoleptic qualities of the oleic acid-enriched milk fat would be expected to be quite different from those of typical milk fat. Butter produced from milk fat with increased oleic acid and decreased palmitic acid is softer at refrigerator temperature (Enjalbert et al., 1997, 2000). Thus, the ratio of 16:0 to 18:1 cis-9 has been used as an index of butter spreadability (Couvreur et al., 2006). This ratio (Table 6) decreased in a quadratic fashion as the amount of infused HOSFA increased. Jenkins (1999) calculated the inverse of this ratio (18:1 cis-9/16:0) and found that it increased linearly as oleic acid in milk fat was enriched by increasing amounts of oleamide in the diet. The changes in milk FA profile also resulted in a quadratic increase in the "health index" (Table 6), described by Chen et al. (2004) as the inverse of the atherogenic index first reported by Ulbricht and Southgate (1991).

Changes in milk fat composition were accompanied by corresponding changes in the LCFA profile of TG in the TG-rich lipoprotein fraction of blood (Table 7). The weight percentages of 14:0, 16:0, 18:1 trans, and 18:2 decreased linearly, whereas 18:0 decreased in a quadratic fashion as the rate of decrease slowed at the higher infusion amounts. The percentage of oleic acid increased linearly; the quadratic effect approached significance (P < 0.07) as the rate of increase tended to slow at infusion of the 2 largest amounts. The changes were similar to those observed in an earlier study in which HOSFA was infused into the abomasum (La-Count et al., 1994).

	CONCLUSIONS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS ACKNOWLEDGEMENTS REFERENCES

 
Increasing the supply of oleic acid to the postruminal digestive tract can markedly change the FA composition of milk fat. The content of oleic acid in milk fat responds linearly to the amount of intestinally absorbable oleic acid, primarily at the expense of 14:0 and 16:0 as well as shorter chain FA. Thus, these data demonstrate that the bovine mammary gland has the ability to produce a remarkably different milk fat when presented with a drastically altered profile of milk fat precursors. Such changes in milk fat composition would be expected to have an impact on the nutritional and processing characteristics of milk fat, which would be important to evaluate.

As the amount of oleic acid provided to the small intestine was increased by abomasal infusion, DMI decreased substantially. These data indicate that oleic acid has suppressive effects on DMI in dairy cows, as observed for linoleic and linolenic acids in previous experiments. Provision of postruminal oleic acid in amounts sufficient to result in large changes in milk fat composition may be difficult to achieve without decreasing DMI and nutrient supply to cows.

	ACKNOWLEDGEMENTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS ACKNOWLEDGEMENTS REFERENCES

 
The authors thank G. Bollero for statistical expertise, which was invaluable in analyses in this experiment. The authors are grateful to D. Bremmer for assistance with abomasal infusions and J. Zhou for assistance with the experiment. We thank C. Luhman of Land O’Lakes Inc. for partial funding and helpful discussions. The gracious donations of HOSFA by the Emery Division of Henkel Chemical Co. (Cincinnati, OH), meat solubles by Milk Specialties Co. (Dundee, IL), and soybean hulls by Archer Daniels Midland Co. (Decatur, IL) are greatly appreciated.

	FOOTNOTES

 
¹ Supported by State of Illinois and USDA-Cooperative State Research, Education, and Extension Service regional research funds appropriated to the Illinois Agricultural Experiment Station, projects W-181 and W-1181; and by Land O’Lakes Inc. (St. Paul, MN).

³ Current address: Department of Animal Science, Cornell University, Ithaca, NY 14853.

⁴ Current address: Departamento de Ingeniería Agroindustrial, Universidad Autónoma de San Luis Potosí, San Luis Potosí, S.L.P., CP 78290, Mexico.

⁵ Current address: Prairie Swine Center, PO Box 21057, Saskatoon, SK S7H 5N9, Canada.

⁶ Deceased.

Received for publication February 18, 2007. Accepted for publication July 23, 2007.

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TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS ACKNOWLEDGEMENTS REFERENCES

 


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