Higher efficacy of dietary DHA provided as a phospholipid than as a triglyceride for brain DHA accretion in neonatal piglets

Long-chain PUFAs (LCPUFAs) occur in foods primarily in the natural lipid classes, triacylglycerols (TAGs) or phospholipids (PLs). We studied the relative efficacy of the neural omega-3 DHA provided in formula to growing piglets as a dose of 13C-DHA bound to either TAG or phosphatidylcholine (PC). Piglets were assigned to identical formula-based diets from early life and provided with TAG-13C-DHA or PC-13C-DHA orally at 16 days. Days later, piglet organs were analyzed for 13C-DHA and other FA metabolites. PC-13C-DHA was 1.9-fold more efficacious for brain gray matter DHA accretion than TAG-13C-DHA, and was similarly more efficacious in gray matter synaptosomes, retina, liver, and red blood cells (RBCs). Liver labeling was greatest, implying initial processing in that organ followed by export to other organs, and suggesting that transfer from gut to bloodstream to liver in part drove the difference in relative efficacy for tissue accretion. Apparent retroconversion to 22:5n-3 was more than double for PC-13C-DHA and was more prominent in neural tissue than in liver or RBCs. These data directly support greater efficacy for PC as a carrier for LCPUFAs compared with TAG, consistent with previous studies of arachidonic acid and DHA measured in other species. Long-chain PUFAs (LCPUFAs) occur in foods primarily in the natural lipid classes, triacylglycerols (TAGs) or phospholipids (PLs). We studied the relative efficacy of the neural omega-3 DHA provided in formula to growing piglets as a dose of 13C-DHA bound to either TAG or phosphatidylcholine (PC). Piglets were assigned to identical formula-based diets from early life and provided with TAG-13C-DHA or PC-13C-DHA orally at 16 days. Days later, piglet organs were analyzed for 13C-DHA and other FA metabolites. PC-13C-DHA was 1.9-fold more efficacious for brain gray matter DHA accretion than TAG-13C-DHA, and was similarly more efficacious in gray matter synaptosomes, retina, liver, and red blood cells (RBCs). Liver labeling was greatest, implying initial processing in that organ followed by export to other organs, and suggesting that transfer from gut to bloodstream to liver in part drove the difference in relative efficacy for tissue accretion. Apparent retroconversion to 22:5n-3 was more than double for PC-13C-DHA and was more prominent in neural tissue than in liver or RBCs. These data directly support greater efficacy for PC as a carrier for LCPUFAs compared with TAG, consistent with previous studies of arachidonic acid and DHA measured in other species. DHA is the most abundant omega-3 FA in the mammalian brain (1Crawford M.A. Casperd N.M. Sinclair A.J. The long chain metabolites of linoleic avid linolenic acids in liver and brain in herbivores and carnivores.Comp. Biochem. Physiol. B. 1976; 54: 395-401Crossref PubMed Scopus (205) Google Scholar), accounting for 8–14% of FAs perinatally in primates (2Diau G.Y. Hsieh A.T. Sarkadi-Nagy E.A. Wijendran V. Nathanielsz P.W. Brenna J.T. The influence of long chain polyunsaturate supplementation on docosahexaenoic acid and arachidonic acid in baboon neonate central nervous system.BMC Med. 2005; 3: 11Crossref PubMed Scopus (162) Google Scholar) and humans (3Makrides M. Neumann M.A. Byard R.W. Simmer K. Gibson R.A. Fatty acid composition of brain, retina, and erythrocytes in breast- and formula-fed infants.Am. J. Clin. Nutr. 1994; 60: 189-194Crossref PubMed Scopus (686) Google Scholar, 4Farquharson J. Cockburn F. Patrick W.A. Jamieson E.C. Logan R.W. Infant cerebral cortex phospholipid fatty-acid composition and diet.Lancet. 1992; 340 ([see comments]): 810-813Abstract PubMed Scopus (494) Google Scholar). In humans, DHA accumulates at an accelerating rate from mid-gestation reaching an inflection point during the first months after birth (5Martinez M. Tissue levels of polyunsaturated fatty acids during early human development.J. Pediatr. 1992; 120: S129-S138Abstract Full Text PDF PubMed Scopus (675) Google Scholar) and continuing well past the plateau of brain weight to reach a plateau around 18 years of age and remain stable to the end of life (6Carver J.D. Benford V.J. Han B. Cantor A.B. The relationship between age and the fatty acid composition of cerebral cortex and erythrocytes in human subjects.Brain Res. Bull. 2001; 56: 79-85Crossref PubMed Scopus (214) Google Scholar). DHA can be synthesized de novo by term and preterm human infants from precursor omega-3 FAs, α-linolenic acid, or EPA (7Carnielli V.P. Wattimena D.J. Luijendijk I.H. Boerlage A. Degenhart H.J. Sauer P.J. The very low birth weight premature infant is capable of synthesizing arachidonic and docosahexaenoic acids from linoleic and linolenic acids.Pediatr. Res. 1996; 40: 169-174Crossref PubMed Scopus (253) Google Scholar, 8Salem Jr, N. Wegher B. Mena P. Uauy R. Arachidonic and docosahexaenoic acids are biosynthesized from their 18-carbon precursors in human infants.Proc. Natl. Acad. Sci. USA. 1996; 93: 49-54Crossref PubMed Scopus (420) Google Scholar, 9Demmelmair H. Sauerwald T. Koletzko B. Richter T. New insights into lipid and fatty acid metabolism via stable isotopes.Eur. J. Pediatr. 1997; 156: S70-S74Crossref PubMed Google Scholar), but the process is generally considered to be inefficient, also challenged by current dietary intakes of omega-6 linoleic acid at relatively high levels (10Brenna J.T. Efficiency of conversion of alpha-linolenic acid to long chain n-3 fatty acids in man.Curr. Opin. Clin. Nutr. Metab. Care. 2002; 5: 127-132Crossref PubMed Scopus (396) Google Scholar, 11Brenna J.T. Salem Jr, N. Sinclair A.J. Cunnane S.C. alpha-Linolenic acid supplementation and conversion to n-3 long-chain polyunsaturated fatty acids in humans.Prostaglandins Leukot. Essent. Fatty Acids. 2009; 80: 85-91Abstract Full Text Full Text PDF PubMed Scopus (663) Google Scholar). Direct measurement of percent incorporation of DHA into the primate brain from precursor α-linolenic acid indicates that it is 7-fold less efficient than preformed DHA. This finding is in contrast to that for arachidonic acid (ARA), present in the brain at similar/comparable levels but not strongly affected by dietary preformed ARA (12Hsieh A.T. Brenna J.T. Dietary docosahexaenoic acid but not arachidonic acid influences central nervous system fatty acid status in baboon neonates.Prostaglandins Leukot. Essent. Fatty Acids. 2009; 81: 105-110Abstract Full Text Full Text PDF PubMed Scopus (42) Google Scholar). Numerous human studies have shown efficacy of dietary preformed DHA to support brain and visual development (13Brenna J.T. Lapillonne A. Background paper on fat and fatty acid requirements during pregnancy and lactation.Ann. Nutr. Metab. 2009; 55: 97-122Crossref PubMed Scopus (85) Google Scholar), and follow-up studies suggest that preformed DHA intake in infancy provides long-term benefits on specific tests of higher cognitive function, although it is widely agreed that no effects can be seen using the Bayley scales, a standard test for normalcy (14Colombo J. Carlson S.E. Cheatham C.L. Shaddy D.J. Kerling E.H. Thodosoff J.M. Gustafson K.M. Brez C. Long-term effects of LCPUFA supplementation on childhood cognitive outcomes.Am. J. Clin. Nutr. 2013; 98: 403-412Crossref PubMed Scopus (138) Google Scholar). While preformed DHA is in human foods and DHA is to of lipid as triacylglycerols phospholipids or In primate human DHA is higher in than in but the of DHA is via of the of of New Scholar). is a of DHA as an in infant development of of DHA for in infant that and infant formula studied the P. M. of long-chain polyunsaturated fatty acids in infant formula on at months of Full Text Full Text PDF PubMed Scopus Google Scholar, P. C. P. of long-chain supplementation in infant formula on cognitive in J. Clin. Nutr. 2013; 98: PubMed Scopus Google Scholar), and infant formula were also widely on the and for and of ARA and DHA. from their DHA and ARA be by In and in studies that TAG in the and consistent with the of the FA of P. J.M. M. C. of human and PubMed Scopus Google Scholar, R.A. with acid in the in the of and in formula-fed piglets to levels of piglets Nutr. 1997; PubMed Scopus Google Scholar), in the in the the H. of polyunsaturated phosphatidylcholine in the Physiol. 1976; PubMed Scopus Google Scholar). of that the and have a of FAs, FAs by and are in a and be for as FAs are into or on the by labeling that as to formula is as efficacious as a for ARA to the brain as in V. G.Y. Nathanielsz P.W. Brenna J.T. of dietary arachidonic acid provided as or phospholipid as for brain arachidonic acid accretion in baboon Res. 2002; PubMed Scopus Google Scholar). We a in piglets using efficacy for the gray matter of the cerebral cortex with DHA. DHA was in using C. Cunnane S.C. A.J. of polyunsaturated fatty acids as for natural PubMed Scopus Google Scholar) and into lipid by The TAG 13C-DHA in the with in the and The was PC with 13C-DHA in the and in the for tissue lipid were from or and The and piglets were by the and at and were with piglets were to with the for at to of were for the on the weight and and not the in the and Piglets were a and were to the and at the piglets were in and were on a formula The FA of the is in DHA was present in low levels in the of TAG and TAG, and DHA are in and for a with the with human and human infant from fat was and in the of TAG the low DHA in TAG, the of TAG provided of DHA compared with from in with human and other mammalian of piglet formula of of in a and DHA in piglet of FA from FA of DHA in a formula was provided for the first and in as in previous studies C. Salem Jr, N. Brenna J.T. arachidonic acid is to dietary arachidonic acid and docosahexaenoic acid in Leukot. Essent. Fatty Acids. Full Text Full Text PDF PubMed Scopus Google Scholar, C. J.M. Salem Jr, N. Brenna J.T. and in piglets of arachidonic acid and J. Nutr. PubMed Scopus Google Scholar). piglets to for was for the first to the piglets and was weight was other in the first and with other human and 16 of 16 piglets of a of piglets were assigned to PC and TAG, with to and age but PC was orally with PC-13C-DHA as TAG was with The piglets were as natural and not a dose but were to the other were by of PC-13C-DHA or TAG-13C-DHA in of and the by The were on the of a of piglet formula and The formula was into and orally to the piglets via formula was by from the were with was also to the piglets at the of a Piglets were but be considered as as their was was to of the formula and the of a of to were by the Piglets were provided with their of to piglets to 13C-DHA in PC and of 13C-DHA in TAG, and the difference was to the of that was after the the DHA dose and in of formula and of piglets were by on a for FA was in with and to red blood cells (RBCs). The of the gray matter on the cerebral cortex was at was for of synaptosomes, and the gray matter was in for FA liver, and were also and were and at for were using to of was to brain tissue were and the at for The was and at for were from the and were as were from of brain gray the liver, and were and FA using a as in M. M. Nathanielsz P.W. Brenna J.T. The influence of early to mid-gestation on long chain polyunsaturated fatty acids in PubMed Scopus Google Scholar). and the and of lipid and J. Biochem. Physiol. PubMed Scopus Google Scholar) was to and were using in of acid in was as an standard to tissue were in and at were analyzed using a with a and as carrier were using the standard and an weight to for and have V. G.Y. Nathanielsz P.W. 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The was the relative of 13C-DHA in the gray matter of the cerebral cortex in the the The in the was for by with considered FAs in the were compared in a in the and were not and were were the and for a no were on 13C-DHA for synaptosomes, retina, liver, and were compared for to the of DHA in TAG and were from the of relative of DHA in formula in a Piglets in at and of and for the and The were as the but in to the other at weight and at These were to of were to The FA of neural tissue is in was in DHA at followed by gray matter and matter acid the DHA omega-6 FAs, was in gray and greater than DHA. piglets have long considered to of linoleic acid, and the n-3 to diets is to support of Google Scholar). These levels are to DHA levels to (1Crawford M.A. Casperd N.M. Sinclair A.J. The long chain metabolites of linoleic avid linolenic acids in liver and brain in herbivores and carnivores.Comp. Biochem. Physiol. B. 1976; 54: 395-401Crossref PubMed Scopus (205) Google Scholar), are composition of piglet in a for the in gray matter and gray matter are in was for DHA and 22:5n-3 The in cerebral cortex gray matter in the was greater than that for the TAG 13C-DHA from the TAG dose was dietary PC was 1.9-fold more efficacious to DHA to the piglet brain compared with in gray matter synaptosomes, also shown in were consistent with the relative The of relative accretion of DHA in the was greater for PC than for The retroconversion was for the and less than of that for the The relative efficacy of PC TAG for the retroconversion of DHA to was gray matter synaptosomes, the of PC TAG was the with a relative efficacy of matter and 13C-DHA were greater than the for liver and RBCs. Liver of the PC compared with of the TAG dose at The relative efficacy was to gray matter and The of 13C-DHA to was greater than for gray relative labeling liver with 13C-DHA that of and a of 13C-DHA the for efficacy of PC TAG was for and for and consistent with in the other with the brain gray matter but in contrast to the liver, 13C-DHA was greater in the than the retroconversion suggesting that retroconversion the liver and in the seen TAG as the of DHA. the relative efficacy of dietary DHA by PC compared with DHA by The that dietary DHA as PC is more for brain gray matter DHA accretion than as The data in matter are consistent with for gray and in other the data is consistent with previous using a to ARA incorporation in V. G.Y. Nathanielsz P.W. Brenna J.T. of dietary arachidonic acid provided as or phospholipid as for brain arachidonic acid accretion in baboon Res. 2002; PubMed Scopus Google Scholar). 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M.A. of is high in low docosahexaenoic PubMed Scopus Google Scholar). of the low dietary is more to previous studies with the early years of the present compared with studies with the relative of 1.9-fold for compared with to current it is relatively by formula DHA levels and the of a dose of it also to greater formula DHA levels as have in primates and humans (12Hsieh A.T. Brenna J.T. Dietary docosahexaenoic acid but not arachidonic acid influences central nervous system fatty acid status in baboon neonates.Prostaglandins Leukot. Essent. Fatty Acids. 2009; 81: 105-110Abstract Full Text Full Text PDF PubMed Scopus (42) Google Scholar, Carlson S.E. K.M. a of the of infant visual as a of the dietary of docosahexaenoic J. Clin. Nutr. PubMed Scopus Google Scholar). Liver 13C-DHA was greater than the 13C-DHA in the gray in contrast to the for the baboon neonate V. G.Y. Nathanielsz P.W. 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The retroconversion also greater in the liver for PC compared with TAG, was a of the liver 13C-DHA than in gray In gray 13C-DHA was greater than in liver the 13C-DHA was synthesized in the liver and to the brain, be These suggest that retroconversion in organs other than the liver and well be more in the brain than in the The piglet long as a for infant of metabolism to humans, and in studies it to the of LCPUFA from N. liver, and red blood in piglets on a formula with and J. Clin. Nutr. PubMed Scopus Google Scholar, J. of and phospholipids as of dietary long-chain polyunsaturated fatty acids in Nutr. 2002; PubMed Scopus Google is more than for human also greater intake and to test than human infants A. R. C. J.M. Brenna J.T. in piglet or organ to dietary long-chain polyunsaturated 2002; 40: PubMed Scopus Google Scholar). have shown that piglet on the of TAG or A. 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In growing the relatively high of indicates for FAs and a for their The of DHA and in gray matter was to that for primates of matter of a of DHA and suggesting that the DHA more the in DHA is the is and the DHA is We that neural DHA levels at dietary of DHA than the very cerebral cortex in primates (2Diau G.Y. Hsieh A.T. Sarkadi-Nagy E.A. Wijendran V. Nathanielsz P.W. Brenna J.T. The influence of long chain polyunsaturate supplementation on docosahexaenoic acid and arachidonic acid in baboon neonate central nervous system.BMC Med. 2005; 3: 11Crossref PubMed Scopus (162) Google data are In stable of DHA bound in the of PC were 1.9-fold more efficacious for of cerebral cortex gray matter than DHA bound to the of These data are generally consistent with previous on other LCPUFAs and on DHA studied in other species. with previous the that PC is a efficacious of DHA and the LCPUFAs of human R. K. fatty acid composition from most in PubMed Scopus Google Scholar). The and for arachidonic acid acid FA long-chain phosphatidylcholine red blood

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