Whole-body β-oxidation of 18:2ω6 and 18:3ω3 in the pig varies markedly with weaning strategy and dietary 18:3ω3

Segregated early weaning (SEW) into a cleaner nursery increases food intake and growth in pigs, presumably because of reduced immune stimulation compared with conventionally reared, nonsegregated pigs (NSW). The aim of the present study was to evaluate the oxidation of linoleic acid (18:2ω6) and α-linolenic acid (18:3ω3) in SEW and NSW pigs. Pigs consumed a control or high 18:3ω3 diet (ω6 PUFA/ω3 PUFA; 21.3 vs. 2.5, respectively) and were weaned at either 14 days old into a SEW nursery or at 21 days old into a conventional NSW nursery. The major acute-phase protein of pigs but not haptoglobin increased in 35-day-old NSW pigs. NSW pigs had 15–25% lower carcass 18:2ω6 and 20–30% lower carcass 18:3ω3 (% composition) at 49 days old. Between 35- and 49-days-old, NSW pigs had a higher whole-body oxidation of 18:2ω6 (40–120%) and 18:3ω3 (30–80%). The high 18:3ω3 diet decreased the whole-body oxidation of 18:2ω6 by 73% and of 18:3ω3 by 63% in NSW pigs.We conclude that moderately cleaner housing SEW significantly decreases 18:2ω6 and 18:3ω3 oxidation in pigs. Segregated early weaning (SEW) into a cleaner nursery increases food intake and growth in pigs, presumably because of reduced immune stimulation compared with conventionally reared, nonsegregated pigs (NSW). The aim of the present study was to evaluate the oxidation of linoleic acid (18:2ω6) and α-linolenic acid (18:3ω3) in SEW and NSW pigs. Pigs consumed a control or high 18:3ω3 diet (ω6 PUFA/ω3 PUFA; 21.3 vs. 2.5, respectively) and were weaned at either 14 days old into a SEW nursery or at 21 days old into a conventional NSW nursery. The major acute-phase protein of pigs but not haptoglobin increased in 35-day-old NSW pigs. NSW pigs had 15–25% lower carcass 18:2ω6 and 20–30% lower carcass 18:3ω3 (% composition) at 49 days old. Between 35- and 49-days-old, NSW pigs had a higher whole-body oxidation of 18:2ω6 (40–120%) and 18:3ω3 (30–80%). The high 18:3ω3 diet decreased the whole-body oxidation of 18:2ω6 by 73% and of 18:3ω3 by 63% in NSW pigs. We conclude that moderately cleaner housing SEW significantly decreases 18:2ω6 and 18:3ω3 oxidation in pigs. The eighteen carbon polyunsaturated fatty acids (PUFA), linoleic acid (18:2ω6), and α-linolenic acid (18:3ω3), are important dietary precursors to longer-chain PUFAs such as arachidonic acid (20:4ω6), eicosapentaenoic acid (20:5ω3), and docosahexaenoic acid (22:6ω3). Several long-chain PUFAs are eicosanoid precursors and also contribute importantly to membrane structure. Despite their important precursor role, 18:2ω6 and 18:3ω3 are primarily β-oxidized for energy (1Cunnane S.C. Anderson M.J. The majority of dietary linoleate in growing rats is β-oxidized or stored in visceral fat.J. Nutr. 1997; 127: 146-152Google Scholar, 2Leyton J. Drury P.J. Crawford M.A. Differential oxidation of saturated and unsaturated fatty acids in vivo in the rat.Br. J. Nutr. 1987; 57: 383-393Google Scholar). Although dietary factors like fasting-refeeding and energy restriction are known to significantly increase the β-oxidation of 18:2ω6 and 18:3ω3, overall little is known about why these two dietarily important fatty acids are mostly β-oxidized. In this study, we were interested in assessing the effect of weaning strategy and diet on 18:2ω6 and 18:3ω3 β-oxidation in young growing pigs. Segregated early weaning (SEW) is a management strategy in which pigs are weaned at 10–14 days old instead of the more common 21 days old and are housed in a cleaner environment compared with nonsegregated weaning (NSW) used in conventional commercial units. SEW pigs eat more and grow faster, and there is some evidence that this is due to reduced antigen exposure, i.e., to less demand on their immune system (3Bassaganya-Riera J.R Hontecillas-Magarzo K. Bregendahl Wannemuehler M.J. Zimmerman D.R. Effects of dietary conjugated linoleic acid in nursery pigs of dirty and clean environments on growth, empty body composition, and immune competence.J. Anim. Sci. 2001; 79: 714-721Google Scholar, 4Patience J.F. Gonyou H.W. L Whittington D. Beltranena E. Rhodes C.S. Van Kessel A.G. Evaluation of site and age of weaning on pig growth performance.J. Anim. Sci. 2000; 78: 1726-1731Google Scholar, 5Dritz S.S. Chengappa M.M. Nelssen J.L. Tokach M.D. Goodband R.D. Nietfeld J.C. Staats J.J. Growth and microbial flora of non-medicated, segregated, early weaned pigs from a commercial swine operation.J. Am. Vet. Med. Assoc. 1996; 208: 711-715Google Scholar, 6Williams N.H. Stahly T.S. Zimmerman D.R. Effect of chronic immune system activation on the rate, efficiency, and composition of growth and lysine needs of pigs fed from 6 to 27 kg.J. Anim. Sci. 1997; 75: 2463-2471Google Scholar, 7Williams N.H. Stahly T.S. Zimmerman D.R. Effect of level of chronic immune system activation on body nitrogen retention, partial efficiency of lysine utilization, and lysine needs of pigs.J. Anim. Sci. 1997; 75: 2472-2480Google Scholar, 8Donham K.J. Association of environmental air contaminants with disease and productivity in swine.Am. J. Vet. Res. 1991; 52: 1723-1730Google Scholar, 9Schinckel A.P. Clark L.K. Stevenson G. Knox K.E. Nielsen J. Grant A.L. Hancock D.L. Turek J. Effects of antigenic challenge on growth and composition of segregated early-weaned pigs.J. Swine Health Prod. 1995; 3: 228-234Google Scholar). We chose this model to further examine parameters affecting 18:2ω6 and 18:3ω3 β-oxidation because there are a few, mostly indirect, studies suggesting a stimulated immune system could contribute significantly to the body’s oxidation of fatty acids. For instance, during severe inflammation, energy expenditure is increased and the respiratory quotient is decreased, indicating an increase in whole-body fat oxidation (10Frankenfield D.C. Wiles 3rd, C.E. Bagley S. Siegel J.H. Relationships between resting and total energy expenditure in injured and septic patients.Crit. Care Med. 1994; 22: 1796-1804Google Scholar, 11Hwang T.L. Huang S.L. Chen M.F. The use of indirect calorimetry in critically ill patients–the relationship of measured energy expenditure to Injury Severity Score, Septic Severity Score, and APACHE II Score.J. Trauma. 1993; 34: 247-251Google Scholar, 12Al-Jaouni R. Hebuterne X. Pouget I. Rampal P. Energy metabolism and substrate oxidation in patients with Crohn’s disease.Nutrition. 2000; 16: 173-178Google Scholar, 13Stoner H.B. Little R.A. Frayn K.N. Elebute A.E. Tresadern J. Gross E. The effect of sepsis on the oxidation of carbohydrate and fat.Br. J. Surg. 1983; 70: 32-35Google Scholar, 14Nanni G. Siegel J.H. Coleman B. Fader P. Castiglione R. Increased lipid fuel dependence in the critically ill septic patient.J. Trauma. 1994; 24: 14-30Google Scholar). The extent to which PUFA such as 18:2ω6 contributes to this inflammation-induced increase in fat oxidation is not known. In a rat model of sepsis caused by puncture of the cecum, 14CO2 recovery 6 h after an oral dose of [14C]18:2n-6 was shown to be 1.5–2 times higher than in controls (15Iriyama K. Kusaka N. Nishiwaki H. Teranishi T. Mori H. Suzuki H. Metabolism of non-protein energy-substrates in septic rats receiving parental nutrition.Int. Surg. 1986; 71: 5-8Google Scholar). As well, rats infused with tumor necrosis factor-α (TNFα) have 10% less 18:2ω6 in carcass triglyceride, suggesting that 18:2ω6 may be mobilized under these conditions (16Raina N. Matsui J. Cunnane S.C. Jeejeebhoy K.N. Effect of tumor necrosis factor a on triglyceride and phospholipid content and fatty acid composition of liver and carcass in rats.Lipids. 1995; 30: 713-718Google Scholar). Hence, we postulated that β-oxidation of 18:2ω6 and 18:3ω3 may decrease in animals undergoing a reduced immune challenge. The objective of the present study was therefore to assess whole-body PUFA balance in NSW and SEW pigs consuming a conventional compared with an increased level of dietary 18:3ω3. Whole-body PUFA balance was chosen as the method to study 18:2ω6 and 18:3ω3 oxidation because, with this method, β-oxidation is determined in relation to the intake of 18:2ω6 or 18:3ω3 over several days to weeks, thus giving a long term comparison between PUFA utilization as fuels versus incorporation into tissue membrane structure or as long chain PUFA precursors (1Cunnane S.C. Anderson M.J. The majority of dietary linoleate in growing rats is β-oxidized or stored in visceral fat.J. Nutr. 1997; 127: 146-152Google Scholar). We hypothesized that SEW pigs would have lower whole-body 18:2ω6 and 18:3ω3 β-oxidation as a result of less immune stimulation due to being housed in a cleaner environment with lower antigen exposure. In view of the anticipated higher oxidation of 18:3ω3 in the NSW pigs, we wanted to assess whether raised 18:3ω3 intake would influence 18:2ω6 and 18:3ω3 balance, especially in the NSW pigs. In the pig, the plasma acute-phase proteins, haptoglobin, and major acute-phase protein of pigs (pigMAP), are sensitive indicators of inflammation (17Heegaard P.M. Klausen J. Nielsen J.P. Gonzalez-Ramon N. Pineiro M. Lampreave F. Alava M.A. The porcine acute phase response to infection with Actinobacillus pleuropneumoniae. Haptoglobin, C-reactive protein, major acute phase protein and serum amyloid A protein are sensitive indicators of infection.Comp. Biochem. Physiol. B Biochem. Mol. Biol. 1998; 119: 365-373Google Scholar). Therefore, in the present study, haptoglobin and pigMAP were determined at various times before and after weaning. Pregnant Yorkshire-Landrace sows (Maple Leaf Foods Agresearch, Burford, ON) were randomly fed either a control diet or a diet high in 18:3ω3 from ∼1 week prior to parturition until weaning. The diets consisted of base commercial pig feed (Shur-Gain Feed # 694, Guelph, ON) containing 477 g/kg of corn, 270 g/kg of soy bean meal, 75 g/kg of wheat middlings, 74 g/kg of whey powder, 36.2 g/kg of fish meal, 10 g/kg of limestone, 7 g/kg of dicalcium phosphate, 3.3 g/kg of salt, and 17.6 g/kg of a vitamin/mineral supplement. The control diet consisted of the base pig feed supplemented with 50 g/kg of sunflower oil, while the high 18:3ω3 diet consisted of the same base pig feed supplemented with 15 g/kg of sunflower oil and 35 g/kg of flaxseed oil. The fatty acid profile of the two diets is shown in Table 1. The piglets in the present study suckled from their respective sows consuming either the control or high-18:3ω3 diet. At 14 days old, 12 suckling pigs per dietary treatment were randomly allocated to either the SEW or NSW treatment. SEW pigs were weaned at 14 days old into a “clean” nursery while NSW pigs were weaned at 21 days old into a conventional nursery. The SEW nursery was made cleaner by segregating pigs in this study from all other pigs except for littermates, while NSW pigs remained in the same nursery as the sow and nonlittermates (3Bassaganya-Riera J.R Hontecillas-Magarzo K. Bregendahl Wannemuehler M.J. Zimmerman D.R. Effects of dietary conjugated linoleic acid in nursery pigs of dirty and clean environments on growth, empty body composition, and immune competence.J. Anim. Sci. 2001; 79: 714-721Google Scholar, 9Schinckel A.P. Clark L.K. Stevenson G. Knox K.E. Nielsen J. Grant A.L. Hancock D.L. Turek J. Effects of antigenic challenge on growth and composition of segregated early-weaned pigs.J. Swine Health Prod. 1995; 3: 228-234Google Scholar). After weaning, pigs consumed diets with the same 18:3ω3 content as their respective sows until the end of the study. Pigs were anesthetized and killed at 14, 35, or 49 days old for tissue proximate and fatty acid analysis. Blood samples were anticoagulated with citrate. Organ distribution of fatty acids was evaluated in liver, brain, viscera, and carcass. Liver, brain, viscera, and carcass were completely homogenized four times using a Hobart Grinder with 0.12 cm dye. An 80 g sample of the carcass homogenate was freeze dried for proximate analysis. A 5 g sample of the liver, brain, viscera, and carcass homogenate were stored at −20°C for fatty acid analysis. The term “whole-body” refers to the carcass, brain, liver, and viscera combined, while “carcass” refers to whole-body minus the liver, brain, and viscera.TABLE 1Fatty acid profile of the control and high 18:3ω3 pig feedsaPercentage of total fatty acids >12 carbons.Fatty AcidControlHigh 18:3ω3Sum SFA14.514.3Sum MUFA21.021.618:3ω31.917.8Sum of other ω3 PUFA<0.1<0.118:2ω661.945.4Sum of other ω6 PUFA<0.1<0.1Total Fat (mg/g)7676SFA, saturated fatty acid; MUFA, monounsaturated fatty acid; PUFA, polyunsaturated fatty acid.a Percentage of total fatty acids >12 carbons. Open table in a new tab SFA, saturated fatty acid; MUFA, monounsaturated fatty acid; PUFA, polyunsaturated fatty acid. Carcass dry matter content was determined by weighing before and after 2 h at 100°C in a drying oven. Dried samples were then analyzed for fat, protein, and ash, according to the American Oil Chemists’ Society method Ba 3–38 and the Association of Official Analytical Chemists methods 990.03 and 925.23, respectively (18American Oil Chemists' SocietyOfficial methods and recommended practices of the AOCS.5th ed. American Oil Chemists' Society, Champaign, Ill1998Google Scholar, 19Association of Official Analytical ChemistsAOAC Official Methods of Analysis.16th ed. Association of Analytical Chemists, Washington DC1995Google Scholar). Total lipids of plasma and homogenized samples of liver, carcass, viscera, and brain were extracted into chloroform-methanol (2:1, v/v). Nonesterified heptadecanoic acid (Sigma, St. Louis, MO) was added as an internal standard to an aliquot of the total fatty acid extract to quantitate total lipids. Total lipids were then recovered and saponified in methanolic potassium hydroxide (60 g potassium hydroxide/l-methanol) for 1 h at 100°C and the fatty acids were converted to fatty acid methyl esters using 14% boron triflouride-methanol at 100°C for 30 min (Sigma) under nitrogen (20Cunnane S.C. Differential utilization of long chain fatty acids during fasting-induced triacylglycerol depletion. III. Comparison of ω3 and ω6 fatty acids in rat plasma and liver.Biochim. Biophys. Acta. 1990; 1036: 64-70Google Scholar). Fatty acid methyl esters were analyzed by gas liquid chromatography using a capillary column ( JandW Scientific DB-23, 30 m × 0.25 mm, in a gas liquid with sample and and Total lipid fatty acids were on the of the in of the internal standard added to and pigMAP were with on with for pig haptoglobin and pigMAP were by with haptoglobin and of of F. of could be and in which were used to The of the respective was determined from the at the of Health and on the at and as units. were with of protein in the conditions as from a standard of versus known of as a E. H.W. M.A. in and major plasma in and with by 22: Scholar). Whole-body fatty acid oxidation was determined as according to fatty acid was not but a of of fatty acid intake was used (1Cunnane S.C. Anderson M.J. The majority of dietary linoleate in growing rats is β-oxidized or stored in visceral fat.J. Nutr. 1997; 127: 146-152Google Scholar). intake and fatty acid were measured between 35 and 49 days old. are as were made using with weaning and and diet and high as the and sow as a was used to the of weaning, and weaning by diet were made using were using A of less than was to be for and were using the SEW pigs consumed more feed between 35 and 49 days old than NSW pigs, a in the body of SEW pigs at 49 days old Table body and feed at 14 days old and 6 pigs per at 35 and 49 intake from 35 to 49 days old segregated early nonsegregated not diet weaning diet by weaning at 14 days old and 6 pigs per at 35 and 49 Feed intake from 35 to 49 days old Open table in a new tab segregated early nonsegregated not diet weaning diet by weaning was effect of diet on plasma haptoglobin or pigMAP at 14 days old At 35 days old, SEW pigs had lower of pigMAP but not haptoglobin were in haptoglobin or pigMAP at 49 days old. At 35 days old, SEW pig more but less fat, less protein, less ash, less and less vs. not were in the proximate composition of pigs. At 49 days old, weaning strategy had effect on plasma total lipid fatty acid NSW and SEW pigs consuming the high 18:3ω3 diet had higher of plasma 18:3ω3 and but not and had lower of 18:2ω6 and At 49 days old, NSW pigs consuming the control diet 18:3ω3 had higher total fatty acids in liver total lipids Pigs consuming the high 18:3ω3 diet had higher carcass 18:3ω3 and but lower 18:2ω6 and to pigs consuming the control diet. At 49 days old, SEW pig more ω3 and ω6 PUFA but less saturated and monounsaturated fatty acids than NSW pigs As well, SEW pigs consuming the high 18:3ω3 diet had higher ω3 PUFA but lower 18:2ω6 in the carcass. was with pigMAP 2 and haptoglobin 2 while plasma was with pigMAP 2 and haptoglobin 2 not acid composition of pig plasma total AcidControlHigh of total fatty acids >12 ω3 of fatty acids more than ω6 of fatty acids more than segregated early nonsegregated SFA, saturated fatty MUFA, monounsaturated fatty PUFA, polyunsaturated fatty not diet weaning Percentage of total fatty acids >12 of fatty acids more than Open table in a new tab acid composition of pig liver total AcidControlHigh of total fatty acids 6 per ω3 of fatty acids more than ω6 of fatty acids more than Fatty extracted fatty acids on liver segregated early nonsegregated SFA, saturated fatty MUFA, monounsaturated fatty PUFA, polyunsaturated fatty not diet weaning diet by weaning Percentage of total fatty acids 6 per of fatty acids more than Total extracted fatty acids on liver Open table in a new tab acid composition of pig carcass total AcidControlHigh of total fatty acids 6 per ω3 of fatty acids more than shown ω6 of fatty acids more than shown Percentage of total fatty acids 6 per of fatty acids more than shown Open table in a new tab segregated early nonsegregated SFA, saturated fatty MUFA, monounsaturated fatty PUFA, polyunsaturated fatty not diet weaning segregated early nonsegregated SFA, saturated fatty MUFA, monounsaturated fatty PUFA, polyunsaturated fatty not diet weaning diet by weaning As a of whole-body of 18:2ω6 and 18:3ω3 between 35 and 49 days old was lower in the SEW pigs by and The high 18:3ω3 diet reduced whole-body of 18:2ω6 and 18:3ω3 in the NSW pigs Whole-body of 18:2ω6 but not 18:3ω3 was with plasma pigMAP 2 not but not with haptoglobin 2 The present study that NSW pigs to all the 18:2ω6 and 18:3ω3 after weaning and that SEW 18:2ω6 and 18:3ω3 SEW to lower whole-body PUFA oxidation in by being a cleaner environment and presumably by immune as by the lower plasma pigMAP in SEW pigs at 35 days old The high 18:3ω3 diet also reduced whole-body oxidation of 18:2ω6 and 18:3ω3 but in the NSW pigs. SEW raised feed intake which the body in this also (3Bassaganya-Riera J.R Hontecillas-Magarzo K. Bregendahl Wannemuehler M.J. Zimmerman D.R. Effects of dietary conjugated linoleic acid in nursery pigs of dirty and clean environments on growth, empty body composition, and immune competence.J. Anim. Sci. 2001; 79: 714-721Google Scholar, 5Dritz S.S. Chengappa M.M. Nelssen J.L. Tokach M.D. Goodband R.D. Nietfeld J.C. Staats J.J. Growth and microbial flora of non-medicated, segregated, early weaned pigs from a commercial swine operation.J. Am. Vet. Med. Assoc. 1996; 208: 711-715Google Scholar, 9Schinckel A.P. Clark L.K. Stevenson G. Knox K.E. Nielsen J. Grant A.L. Hancock D.L. Turek J. Effects of antigenic challenge on growth and composition of segregated early-weaned pigs.J. Swine Health Prod. 1995; 3: 228-234Google Scholar). feed intake after weaning may have on body the in plasma pigMAP was and by the the pigs were 49 days old. Although not measured in the present study, such as would be to be lower in the SEW compared with NSW pigs, which would increase and growth in the P.J. necrosis in swine after oral or respiratory challenge with or J. Vet. Res. 1995; Scholar). The higher total fatty acid content of the liver in NSW pigs on the control diet is with other of infection T. H. K. N. K. N. versus polyunsaturated fatty acids in 1998; Scholar, S. H. R. of a lipid containing fish oil the fatty liver of 1995; 30: Scholar). 18:3ω3 intake significantly reduced total fatty acid in NSW pig mostly by ω6 PUFA, an effect with that raised intake of fatty acid in the liver of rats infused with and T. H. K. N. K. N. versus polyunsaturated fatty acids in 1998; Scholar, S. H. R. of a lipid containing fish oil the fatty liver of 1995; 30: Scholar). SEW pigs had higher carcass of 18:2ω6 and 18:3ω3, but lower of and in weaning strategy and ω3 PUFA compared with SEW carcass PUFA, to reduced whole-body of 18:2ω6 and 18:3ω3. higher 18:3ω3 in NSW pigs 18:2ω6 and 18:3ω3 oxidation that some of the PUFA from the carcass to PUFA in the liver of the NSW pigs. to be to the as in of infection D. E. in patients receiving growth of triglyceride Surg. 1996; Scholar). for the lower carcass PUFA in NSW pigs could to the of sensitive sensitive is for fatty acids from into the In studies with have shown that stimulated with sensitive PUFA into the polyunsaturated fatty acids from Scholar). the present study is not higher 18:3ω3 intake the of SEW on PUFA 18:3ω3 not decrease the acute-phase protein response at measured plasma was and was with the of haptoglobin and pigMAP that are to from to decrease as by with for eicosanoid D. from arachidonic and eicosapentaenoic acids 1993; Scholar, P. in of response to and by fatty 1997; Scholar, B. S. J. polyunsaturated fatty acids and on the of and immune an 1990; Scholar). is also a for the of in fat metabolism D. Fatty acids and immune new in for and Nutr. 2000; Scholar, H. M. The to inflammation 1996; Scholar). 18:3ω3 is converted to which may some of the of 18:3ω3 of of α-linolenic acid to long chain fatty acids in Nutr. Scholar, S.C. Metabolism and of α-linolenic acid in Cunnane in Champaign, Scholar). In SEW in growth, less total fat in the liver, higher PUFA in the carcass, and a decrease in the whole-body of 18:2ω6 and 18:3ω3. whole-body oxidation of 18:2ω6 and 18:3ω3, dietary 18:3ω3 some of the in PUFA metabolism by The by which this is not known. We conclude that moderately cleaner housing after weaning (SEW) PUFA effect on PUFA metabolism is to less immune stimulation in the SEW compared with NSW nursery but of this further study. The of The of Open The and and The and and of are for arachidonic acid linoleic acid α-linolenic acid docosahexaenoic acid major acute phase protein of pigs monounsaturated fatty acid nonsegregated weaning acid acid polyunsaturated fatty acid saturated fatty acid segregated early weaning acid

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