Advertisement
Research Article| Volume 85, ISSUE 6, P369-379, December 2011

Differences in preterm and term milk fatty acid compositions may be caused by the different hormonal milieu of early parturition

Published:September 07, 2011DOI:https://doi.org/10.1016/j.plefa.2011.08.001

      Abstract

      Introduction

      The hormonal milieus of pregnancy and lactation are driving forces of nutrient fluxes supporting infant growth and development. The decrease of insulin sensitivity with compensatory hyperinsulinemia with advancing gestation, causes adipose tissue lipolysis and hepatic de novo lipogenesis (DNL).

      Subjects and methods

      We compared fatty acid (FA) contents and FA-indices for enzyme activities between preterm (28–36 weeks) and term (37–42) milks, and between colostrum (2–5 days), transitional (6–15) and mature (16–56) milks. We interpreted FA differences between preterm and term milks, and their changes with lactation, in terms of the well known decrease of insulin sensitivity during gestation and its subsequent postpartum restoration, respectively.

      Results

      Compared with term colostrum, preterm colostrum contained higher indices of DNL in the breast (DNL-breast) and medium chain saturated-FA (MCSAFA), and lower DNL-liver and monounsaturated-FA (MUFA). Preterm milk also had higher docosahexaenoic acid (DHA) in colostrum and transitional milk and higher arachidonic acid (AA) in mature milk. Most preterm-term differences vanished with advancing lactation. In both preterm and term milks, DNL-breast and MCSAFA increased with advancing lactation, while DNL-liver, MUFA, long chain SAFA and AA decreased. DHA decreased in term milk. MUFA was inversely related to MCSAFA in all samples, correlated inversely with PUFA in colostrum and transitional milks, but positively in mature milk. MCSAFA correlated inversely with PUFA in mature milk.

      Conclusion

      Higher maternal insulin sensitivity at preterm birth may be the cause of lower MUFA (a proxy for DNL-liver) and higher MCSAFA (a proxy for DNL-breast) in preterm colostrum, compared with term colostrum. Restoring insulin sensitivity after delivery may be an important driving force for milk FA-changes in early lactation.

      Abbreviations:

      AA (arachidonic acid), ALA (α-linolenic acid), DHA (docosahexaenoic acid), DNL (de novo lipogenesis, ΣDNL, sum of de novo synthesized fatty acids), Elovl-6 (elongation of very long-chain fatty acids family member 6), EFA (essential fatty acids), EPA (eicosapentaenoic acid), FA (fatty acid), D5D (Δ5-desaturase), D6D (Δ6-desaturase), LA (linoleic acid), LCSAFA (long chain saturated fatty acids (≥16:0)), LCP (long chain polyunsaturated fatty acids), LPL (lipoprotein lipase), MCSAFA (medium chain saturated fatty acids (≤14:0)), MUFA (monounsaturated fatty acids), PL (phospholipids), PUFA (polyunsaturated fatty acids, SAFA, saturated fatty acids), SCD (stearoyl-CoA desaturase (Δ9-desaturase)), TG (triglycerides), VLDL (very low density lipoprotein)

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Prostaglandins, Leukotrienes and Essential Fatty Acids
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Neville M.C.
        • Picciano M.F.
        Regulation of milk lipid secretion and composition.
        Annual Review of Nutrition. 1997; 17: 159-183
        • Emken E.A.
        • Adlof R.O.
        • Hachey D.L.
        • Garza C.
        • Thomas M.R.
        • Brownbooth L.
        Incorporation of deuterium-labeled fatty-acids into human-milk, plasma, and lipoprotein phospholipids and cholesteryl esters.
        Journal of lipid Research. 1989; 30: 395-402
        • Thompson B.J.
        • Smith S.
        Biosynthesis of fatty acids by lactating human breast epithelial cells: an evaluation of the contribution to the overall composition of human milk fat.
        Pediatric Research. 1985; 19: 139-143
        • Del Prado M.
        • Villalpando S.
        • Elizondo A.
        • Rodriguez M.
        • Demmelmair H.
        • Koletzko B.
        Contribution of dietary and newly formed arachidonic acid to human milk lipids in women eating a low-fat diet.
        American Journal of Clinical Nutrition. 2001; 74: 242-247
        • Demmelmair H.
        • Baumheuer M.
        • Koletzko B.
        • Dokoupil K.
        • Kratl G.
        Investigation of long-chain polyunsaturated fatty acid metabolism in lactating women by means of stable isotope techniques.
        Advances in Experimental Medicine and Biology. 2001; 501: 169-177
        • Hachey D.L.
        • Thomas M.R.
        • Emken E.A.
        • et al.
        Human lactation—maternal transfer of dietary triglycerides labeled with stable isotopes.
        Journal of Lipid Research. 1987; 28: 1185-1192
        • Fidler N.
        • Sauerwald T.
        • Pohl A.
        • Demmelmair H.
        • Koletzko B.
        Docosahexaenoic acid transfer into human milk after dietary supplementation: a randomized clinical trial.
        Journal of Lipid Research. 2000; 41: 1376-1383
        • Lascelles A.K.
        • Hardwick D.C.
        • Linzell J.L.
        • Mepham T.B.
        The transfer of [3H]stearic acid from chylomicra to milk fat in the goat.
        The Biochemical Journal. 1964; 92: 36-42
        • Read W.W.
        • Lutz P.G.
        • Tashjian A.
        Human milk lipids. II. The influence of dietary carbohydrates and fat on the fatty acids of mature milk. A study in four ethnic groups.
        The American Journal of Clinical Nutrition. 1965; 17: 180-183
        • Francois C.A.
        • Connor S.L.
        • Wander R.C.
        • Connor W.E.
        Acute effects of dietary fatty acids on the fatty acids of human milk.
        The American Journal of Clinical Nutrition. 1998; 67: 301-308
        • Jensen R.G.
        The Lipids of Human Milk. CRC Press, Boca Raton, Florida1989
        • Martyn P.
        • Hansen I.A.
        Initiation of lipogenic enzyme activities in rat mammary glands.
        The Biochemical Journal. 1981; 198: 187-192
        • Harzer G.
        • Haug M.
        • Dieterich I.
        • Gentner P.R.
        Changing patterns of human milk lipids in the course of the lactation and during the day.
        The American Journal of Clinical Nutrition. 1983; 37: 612-621
        • Spear M.L.
        • Bitman J.
        • Hamosh M.
        • Wood D.L.
        • Gavula D.
        • Hamosh P.
        Human mammary gland function at the onset of lactation: medium-chain fatty acid synthesis.
        Lipids. 1992; 27: 908-911
        • Hamosh M.
        • Clary T.R.
        • Chernick S.S.
        • Scow R.O.
        Lipoprotein lipase activity of adipose and mammary tissue and plasma triglyceride in pregnant and lactating rats.
        Biochimica et Biophysica Acta. 1970; 210: 473-482
        • Ramos P.
        • Herrera E.
        Comparative responsiveness to prolonged hyperinsulinemia between adipose-tissue and mammary-gland lipoprotein lipase activities in pregnant rats.
        Early Pregnancy: Biology and Medicine: The Official Journal of the Society for the Investigation of Early Pregnancy. 1996; 2: 29-35
        • Rogers M.P.
        • Zhao X.
        Lipoprotein lipase mRNA levels in adipose tissue in lactation.
        Biochemical Society Transactions. 1996; 24: 169S
        • Koletzko B.
        • Rodriguez-Palmero M.
        Polyunsaturated fatty acids in human milk and their role in early infant development.
        Journal of Mammary Gland Biology and Neoplasia. 1999; 4: 269-284
        • Martin J.C.
        • Bougnoux P.
        • Antoine J.M.
        • Lanson M.
        • Couet C.
        Triacylglycerol structure of human colostrum and mature milk.
        Lipids. 1993; 28: 637-643
        • Bitman J.
        • Wood D.L.
        • Mehta N.R.
        • Hamosh P.
        • Hamosh M.
        Comparison of the phospholipid composition of breast milk from mothers of term and preterm infants during lactation.
        The American Journal of Clinical Nutrition. 1984; 40: 1103-1119
        • Shoji H.
        • Shimizu T.
        • Kaneko N.
        • et al.
        Comparison of the phospholipid classes in human milk in Japanese mothers of term and preterm infants.
        Acta Paediatrica (Oslo, Norway: 1992). 2006; 95: 996-1000
        • Simonin C.
        • Ruegg M.
        • Sidiropoulos D.
        Comparison of the fat content and fat globule size distribution of breast milk from mothers delivering term and preterm.
        The American Journal of Clinical Nutrition. 1984; 40: 820-826
        • Sala-Vila A.
        • Castellote A.I.
        • Rodriguez-Palmero M.
        • Campoy C.
        • Lopez-Sabater M.C.
        Lipid composition in human breast milk from Granada (Spain): changes during lactation.
        Nutrition (Burbank, Los Angeles County, California). 2005; 21: 467-473
        • Rüegg M.
        • Blanc B.
        The particulate constituents of human milk. A review.
        Food Microstructures. 1982; 1: 25-47
        • Rüegg M.
        • Blanc B.
        The fat globule size distribution in human milk.
        Biochimica et Biophysica Acta. 1981; 666: 7-14
        • Al Tamer Y.Y.
        • Mahmood A.A.
        Fatty-acid composition of the colostrum and serum of fullterm and preterm delivering Iraqi mothers.
        European Journal of Clinical Nutrition. 2004; 58: 1119-1124
        • Bokor S.
        • Koletzko B.
        • Decsi T.
        Systematic review of fatty acid composition of human milk from mothers of preterm compared to full-term infants.
        Annals of Nutrition and Metabolism. 2007; 51: 550-556
        • Kovacs A.
        • Funke S.
        • Marosvolgyi T.
        • Burus I.
        • Decsi T.
        Fatty acids in early human milk after preterm and full-term delivery.
        Journal of Pediatric Gastroenterology and Nutrition. 2005; 41: 454-459
        • Luukkainen P.
        • Salo M.K.
        • Nikkari T.
        Changes in the fatty acid composition of preterm and term human milk from 1 week to 6 months of lactation.
        Journal of Pediatric Gastroenterology and Nutrition. 1994; 18: 355-360
        • Marin M.C.
        • Sanjurjo A.L.
        • Sager G.
        • Margheritis C.
        • de Alaniz M.J.
        Fatty acid composition of human milk from mothers of preterm and full-term infants.
        Archivos Argentinos de Pediatria. 2009; 107: 315-320
        • Bitman J.
        • Wood L.
        • Hamosh M.
        • Hamosh P.
        • Mehta N.R.
        Comparison of the lipid composition of breast milk from mothers of term and preterm infants.
        The American Journal of Clinical Nutrition. 1983; 38: 300-312
        • Beijers R.J.
        • Schaafsma A.
        Long-chain polyunsaturated fatty acid content in Dutch preterm breast milk; differences in the concentrations of docosahexaenoic acid and arachidonic acid due to length of gestation.
        Early Human Development. 1996; 44: 215-223
        • Genzel-Boroviczeny O.
        • Wahle J.
        • Koletzko B.
        Fatty acid composition of human milk during the 1st month after term and preterm delivery.
        European Journal of Pediatrics. 1997; 156: 142-147
        • Molto-Puigmarti C.
        • Castellote A.I.
        • Carbonell-Estrany X.
        • Lopez-Sabater M.C.
        Differences in Fat Content and Fatty Acid Proportions Among Colostrum, Transitional, and Mature Milk from Women Delivering Very Preterm, Preterm, and Term Infants. Clinical Nutrition (Edinburgh, Lothian), 2010
        • Rueda R.
        • Garcia-Salmeron J.L.
        • Maldonado J.
        • Gil A.
        Changes during lactation in ganglioside distribution in human milk from mothers delivering preterm and term infants.
        Biological Chemistry. 1996; 377: 599-601
        • Ehrenkranz R.A.
        • Ackerman B.A.
        • Nelli C.M.
        Total lipid content and fatty acid composition of preterm human milk.
        Journal of Pediatric Gastroenterology and Nutrition. 1984; 3: 755-758
        • Read W.W.
        • Sarrif A.
        Human milk lipids. I. Changes in fatty acid composition of early colostrum.
        The American Journal of Clinical Nutrition. 1965; 17: 177-179
        • Gibson R.A.
        • Kneebone G.M.
        Fatty acid composition of human colostrum and mature breast milk.
        The American Journal of Clinical Nutrition. 1981; 34: 252-257
        • Guesnet P.
        • Antoine J.M.
        • Rochette de Lempdes J.B.
        • Galent A.
        • Durand G.
        Polyunsaturated fatty acid composition of human milk in France: changes during the course of lactation and regional differences.
        European Journal of Clinical Nutrition. 1993; 47: 700-710
        • Lammi-Keefe C.J.
        • Jensen R.G.
        Lipids in human milk: a review. 2: composition and fat-soluble vitamins.
        Journal of Pediatric Gastroenterology and Nutrition. 1984; 3: 172-198
        • Hadden D.R.
        • McLaughlin C.
        Normal and abnormal maternal metabolism during pregnancy.
        Seminars in Fetal and Neonatal Medicine. 2009; 14: 66-71
        • Herrera E.
        • Amusquivar E.
        Lipid metabolism in the fetus and the newborn.
        Diabetes—Metabolism Research and Reviews. 2000; 16: 202-210
        • Hudgins L.C.
        • Baday A.
        • Hellerstein M.K.
        • et al.
        The effect of dietary carbohydrate on genes for fatty acid synthase and inflammatory cytokines in adipose tissues from lean and obese subjects.
        The Journal of Nutritional Biochemistry. 2008; 19: 237-245
        • Al M.D.
        • van Houwelingen A.C.
        • Kester A.D.
        • Hasaart T.H.
        • de Jong A.E.
        • Hornstra G.
        Maternal essential fatty acid patterns during normal pregnancy and their relationship to the neonatal essential fatty acid status.
        The British Journal of Nutrition. 1995; 74: 55-68
        • Otto S.J.
        • van Houwelingen A.C.
        • Badart-Smook A.
        • Hornstra G.
        Changes in the maternal essential fatty acid profile during early pregnancy and the relation of the profile to diet.
        The American Journal of Clinical Nutrition. 2001; 73: 302-307
        • Vlaardingerbroek H.
        • Hornstra G.
        Essential fatty acids in erythrocyte phospholipids during pregnancy and at delivery in mothers and their neonates: comparison with plasma phospholipids.
        Prostaglandins, Leukotrienes, and Essential Fatty Acids. 2004; 71: 363-374
        • Stark K.D.
        • Beblo S.
        • Murthy M.
        • et al.
        Comparison of bloodstream fatty acid composition from African–American women at gestation, delivery, and postpartum.
        Journal of Lipid Research. 2005; 46: 516-525
        • Ryan E.A.
        • O'Sullivan M.J.
        • Skyler J.S.
        Insulin action during pregnancy.
        Studies with the Euglycemic Clamp Technique. Diabetes. 1985; 34: 380-389
        • Kuipers R.S.
        • Luxwolda M.F.
        • Sango W.S.
        • et al.
        Postpartum changes in maternal and infant erythrocyte fatty acids are likely to be driven by restoring insulin sensitivity and DHA status.
        Medical Hypotheses. 2011; 76: 794-801
      1. M.F. Luxwolda, R.S. Kuipers, W.S. Sango, G. Kwesigabo, D.A.J. Dijck-Brouwer, F.A. Muskiet, A maternal erythrocyte DHA content of approximately 6 g% is the DHA status at which intrauterine DHA biomagnifications turns into bioattenuation and postnatal infant DHA equilibrium is reached, submitted for publication.

        • Kuipers R.S.
        • Luxwolda M.F.
        • Sango W.S.
        • Kwesigabo G.
        • Dijck-Brouwer D.A.
        • Muskiet F.A.
        Maternal DHA equilibrium during pregnancy and lactation is reached at an erythrocyte DHA content of 8 g/100 g fatty acids.
        The Journal of Nutrition. 2011; 141: 418-427
      2. R.S. Kuipers, M.F. Luxwolda, W.S. Sango, G. Kwesigabo, D.A.J. Dijck-Brouwer, F.A. Muskiet. Fatty acid compositions of preterm and term colostrum, transitional and mature milk in an African population with high freshwater fish intake, submitted for publication.

        • Paton C.M.
        • Ntambi J.M.
        Biochemical and physiological function of stearoyl-CoA desaturase.
        American Journal of Physiology—Endocrinology and Metabolism. 2009; 297: E28-E37
        • Matsuzaka T.
        • Shimano H.
        Elovl6: a new player in fatty acid metabolism and insulin sensitivity.
        Journal of Molecular Medicine—JMM. 2009; 87: 379-384
        • Vessby B.
        • Gustafsson I.B.
        • Tengblad S.
        • Boberg M.
        • Andersson A.
        Desaturation and elongation of fatty acids and insulin action.
        Lipids and Insulin Resistance: The Role of Fatty Acid Metabolism and Fuel Partitioning. 2002; 967: 183-195
        • Vessby B.
        Dietary fat, fatty acid composition in plasma and the metabolic syndrome.
        Current Opinion in Lipidology. 2003; 14: 15-19
        • Brenner R.R.
        Hormonal modulation of delta 6 and delta 5 desaturases: case of diabetes.
        Prostaglandins Leukotrienes and Essential Fatty Acids. 2003; 68: 151-162
        • Das U.N.
        A defect in the activity of delta(6) and delta(5) desaturases may be a factor predisposing to the development of insulin resistance syndrome.
        Prostaglandins Leukotrienes and Essential Fatty Acids. 2005; 72: 343-350
        • Attie A.D.
        • Krauss R.M.
        • Gray-Keller M.P.
        • et al.
        Relationship between stearoyl-CoA desaturase activity and plasma triglycerides in human and mouse hypertriglyceridemia.
        Journal of Lipid Research. 2002; 43: 1899-1907
        • Corpeleijn E.
        • Feskens E.J.
        • Jansen E.H.
        • et al.
        Improvements in glucose tolerance and insulin sensitivity after lifestyle intervention are related to changes in serum fatty acid profile and desaturase activities: the SLIM study.
        Diabetologia. 2006; 49: 2392-2401
        • Chong M.F.
        • Hodson L.
        • Bickerton A.S.
        • et al.
        Parallel activation of de novo lipogenesis and stearoyl-CoA desaturase activity after 3 d of high-carbohydrate feeding.
        The American Journal of Clinical Nutrition. 2008; 87: 817-823
        • Zhou Y.E.
        • Egeland G.M.
        • Meltzer S.J.
        • Kubow S.
        The association of desaturase 9 and plasma fatty acid composition with insulin resistance-associated factors in female adolescents.
        Metabolism: Clinical and Experimental. 2009; 58: 158-166
        • Sjogren P.
        • Sierra-Johnson J.
        • Gertow K.
        • et al.
        Fatty acid desaturases in human adipose tissue: relationships between gene expression, desaturation indexes and insulin resistance.
        Diabetologia. 2008; 51: 328-335
        • Flowers M.T.
        The delta 9 fatty acid desaturation index as a predictor of metabolic disease.
        Clinical Chemistry. 2009; 55: 2071-2073
        • Jump D.B.
        N-3 polyunsaturated fatty acid regulation of hepatic gene transcription.
        Current Opinion in Lipidology. 2008; 19: 242-247
        • Haig D.
        Genetic conflicts in human pregnancy.
        The Quarterly Review of Biology. 1993; 68: 495-532
        • Handwerger S.
        • Freemark M.
        The roles of placental growth hormone and placental lactogen in the regulation of human fetal growth and development.
        Journal of Pediatric Endocrinology and Metabolism: JPEM. 2000; 13: 343-356
        • Montelongo A.
        • Lasuncion M.A.
        • Pallardo L.F.
        • Herrera E.
        Longitudinal study of plasma lipoproteins and hormones during pregnancy in normal and diabetic women.
        Diabetes. 1992; 41: 1651-1659
        • Damjanovic S.S.
        • Stojic R.V.
        • Lalic N.M.
        • et al.
        Relationship between basal metabolic rate and cortisol secretion throughout pregnancy.
        Endocrine. 2009; 35: 262-268
        • Landgraf R.
        • Landraf-Leurs M.M.
        • Weissmann A.
        • Horl R.
        • von Werder K.
        • Scriba P.C.
        Prolactin: a diabetogenic hormone.
        Diabetologia. 1977; 13: 99-104
        • Butte N.F.
        • Hopkinson J.M.
        • Nicolson M.A.
        Leptin in human reproduction: serum leptin levels in pregnant and lactating women.
        The Journal of Clinical Endocrinology and Metabolism. 1997; 82: 585-589
        • Kirwan J.P.
        • Mouzon Hauguel-De
        • Lepercq J.
        • et al.
        TNF-alpha is a predictor of insulin resistance in human pregnancy.
        Diabetes. 2002; 51: 2207-2213
        • Lain K.Y.
        • Catalano P.M.
        Factors that Affect Maternal Insulin Resistance and Modify Fetal Growth and Body Composition. 2006; 4: 91-100
        • Warensjo E.
        • Riserus U.
        • Vessby B.
        Fatty acid composition of serum lipids predicts the development of the metabolic syndrome in men.
        Diabetologia. 2005; 48: 1999-2005
        • Kuipers R.S.
        • Smit E.N.
        • van der Meulen J.
        • Janneke Dijck-Brouwer D.A.
        • Rudy Boersma E.
        • Muskiet F.A.
        Milk in the island of Chole (Tanzania) is high in lauric, myristic, arachidonic and docosahexaenoic acids, and low in linoleic acid reconstructed diet of infants born to our ancestors living in tropical coastal regions.
        Prostaglandins, Leukotrienes, and Essential Fatty Acids. 2007; 76: 221-233
        • van der Westhuyzen J.
        • Chetty N.
        • Atkinson P.M.
        Fatty acid composition of human milk from South African black mothers consuming a traditional maize diet.
        European Journal of Clinical Nutrition. 1988; 42: 213-220
        • Koletzko B.
        • Thiel I.
        • Abiodun P.O.
        The fatty acid composition of human milk in Europe and Africa.
        The Journal of Pediatrics. 1992; 120: S62-S70
        • Lapillonne A.
        • Jensen C.L.
        Reevaluation of the DHA requirement for the premature infant.
        Prostaglandins, Leukotrienes, and Essential Fatty Acids. 2009; 81: 143-150
        • Fleith M.
        • Clandinin M.T.
        Dietary PUFA for preterm and term infants: review of clinical studies.
        Critical Reviews in Food Science and Nutrition. 2005; 45: 205-229
        • Da Costa T.H.
        • Williamson D.H.
        Effects of exogenous insulin or vanadate on disposal of dietary triacylglycerols between mammary gland and adipose tissue in the lactating rat: insulin resistance in white adipose tissue.
        The Biochemical Journal. 1993; 290: 557-561
        • Bitman J.
        • Hamosh M.
        • Hamosh P.
        • et al.
        Milk composition and volume during the onset of lactation in a diabetic mother.
        The American Journal of Clinical Nutrition. 1989; 50: 1364-1369
        • Steiner G.
        • Myher J.J.
        • Kuksis A.
        Milk and plasma lipid composition in a lactating patient with type I hyperlipoproteinemia.
        The American Journal of Clinical Nutrition. 1985; 41: 121-128
        • Gibson R.A.
        • Kneebone G.M.
        A lack of correlation between linoleate and arachidonate in human breast milk.
        Lipids. 1984; 19: 469-471
        • Minda H.
        • Kovacs A.
        • Funke S.
        • et al.
        Changes of fatty acid composition of human milk during the first month of lactation: a day-to-day approach in the first week.
        Annals of Nutrition and Metabolism. 2004; 48: 202-209
        • Cunnane S.C.
        • Armstrong J.K.
        Long-chain fatty acid composition of maternal liver lipids during pregnancy and lactation in the rat: comparison of triglyceride to phospholipid.
        The Journal of Nutrition. 1990; 120: 338-345
        • Huiskes V.J.B.
        • Kuipers R.S.
        • Velzing-Aarts F.V.
        • Dijck-Brouwer D.A.J.
        • van der Meulen J.
        • Muskiet F.A.J.
        Higher de novo synthesized fatty acids and lower omega 3-and omega 6-long-chain polyunsaturated fatty acids in umbilical vessels of women with preeclampsia and high fish intakes.
        Prostaglandins Leukotrienes and Essential Fatty Acids. 2009; 80: 101-106
        • Martinez M.
        • Mougan I.
        Fatty acid composition of human brain phospholipids during normal development.
        Journal of Neurochemistry. 1998; 71: 2528-2533
        • Innis S.M.
        Essential fatty acid transfer and fetal development.
        Placenta. 2005; 26: S70-S75
        • Manley B.J.
        • Makrides M.
        • Collins C.T.
        • et al.
        High-dose docosahexaenoic acid supplementation of preterm infants: respiratory and allergy outcomes.
        Pediatrics. 2011; 128: e71-e77
        • Hansen H.S.
        • Jensen B.
        Essential function of linoleic acid esterified in acylglucosylceramide and acylceramide in maintaining the epidermal water permeability barrier. Evidence from feeding studies with oleate, linoleate, arachidonate, columbinate and alpha-linolenate.
        Biochimica et Biophysica Acta. 1985; 834: 357-363
        • Wertz P.W.
        • Stover P.M.
        • Downing D.T.
        A survey of polar and nonpolar lipids from epidermis and epidermal appendages of the chicken (Gallus domesticus).
        Comparative Biochemistry and Physiology. B, Comparative Biochemistry. 1986; 84: 203-206
        • Chiou Y.B.
        • Blume-Peytavi U.
        Stratum corneum maturation. A review of neonatal skin function.
        Skin Pharmacology and Physiology. 2004; 17: 57-66
        • Li W.
        • Sandhoff R.
        • Kono M.
        • et al.
        Depletion of ceramides with very long chain fatty acids causes defective skin permeability barrier function, and neonatal lethality in ELOVL4 deficient mice.
        International Journal of Biological Sciences. 2007; 3: 120-128
        • Uchida Y.
        • Holleran W.M.
        Omega-O-acylceramide, a lipid essential for mammalian survival.
        Journal of Dermatological Science. 2008; 51: 77-87
        • Jensen R.G.
        • Clark R.M.
        • Dejong F.A.
        • Hamosh M.
        • Liao T.H.
        • Mehta N.R.
        The lipolytic triad – human lingual, breast-milk, and pancreatic lipases – physiological implications of their characteristics in digestion of dietary fats.
        Journal of pediatric gastroenterology and nutrition. 1982; 1: 243-255