Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-13T08:01:54.877Z Has data issue: false hasContentIssue false

Maternal diet high in fat reduces docosahexaenoic acid in liver lipids of newborn and sucking rat pups

Published online by Cambridge University Press:  09 March 2007

K. Ghebremeskel
Affiliation:
Institute of Brain Chemistry and Human Nutrition, The University of North London, N7 8DB, UK
D. Bitsanis
Affiliation:
Institute of Brain Chemistry and Human Nutrition, The University of North London, N7 8DB, UK
E. Koukkou
Affiliation:
Department of Endocrinology and Diabetes, United Dental and Medical Schools, St Thomas's Hospital, London SE1 7EH, UK
C. Lowy
Affiliation:
Department of Endocrinology and Diabetes, United Dental and Medical Schools, St Thomas's Hospital, London SE1 7EH, UK
L. Poston
Affiliation:
Department of Obstetrics and Gynaecology, Fetal Health Research Group, United Medical and Dental Schools, St Thomas's Hospital, London SE1 7EH, UK
M. A. Crawford*
Affiliation:
Institute of Brain Chemistry and Human Nutrition, The University of North London, N7 8DB, UK
*
*Corresponding author: Professor M. A. Crawford, fax +44 (0)171 753 3164, email michael@macrawf.demon.co.uk
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

The effect of a maternal diet high in fat, similar to Western foods, and of diabetes on liver essential fatty acid composition of the mother and the newborn and sucking pups was investigated. Female Sprague-Dawley rats were fed on either a low-fat (42 g/kg) or a high-fat (329 g/kg) diet for 10 d before mating, throughout pregnancy and post-partum. On the first day of pregnancy, diabetes was induced by intravenous administration of streptozotocin in half the animals from the two diet groups. Half the pups were killed at birth, and the remaining pups and mothers at days 15 and 16 respectively. At birth, there was a significant reduction in the proportions of docosahexaenoic acid (DHA) in the liver phosphoglycerols and neutral lipids of the pups of both high-fat control and diabetic mothers compared with those of low-fat control and diabetic mothers. Diabetes decreased arachidonic (AA) and linoleic acid values in both the low- and high-fat groups at birth. The sucking pups of both the high-fat control and diabetic mothers exhibited a significant reduction in DHA and a concomitant compensatory increase in AA and a lowering in DHA–AA balance. In the mothers, the high-fat diet significantly increased the proportions of DHA in ethanolamine phosphoglycerols but had no observable effect in choline phosphoglycerols and neutral lipids. In the fetus the DHA level (g/100 g total fatty acids) was disproportionately reduced by the maternal high-fat diet. The adverse effect of the high-fat diet on the level of DHA (g/100 g total fatty acids) was greater in the neonate (and by implication the fetus) than in the sucking pups or mothers. It is concluded that a distortion of the biochemistry is induced in the offspring through a maternal high-fat diet, without genetic predisposition.

Type
Research Article
Copyright
Copyright © The Nutrition Society 1999

References

Al, MDM, Houwelingen, AC, Kester, ADM, Hasaart, THM, De-Jong, AET & Hornstra, G (1995) Maternal essential fatty acid patterns during normal pregnancy and relationship to neonatal essential fatty acid status. British Journal of Nutrition 74, 5568.CrossRefGoogle ScholarPubMed
Anderson, RE & Maude, MB (1972) Lipids of ocular tissues: VII. The effects of essential fatty acid deficiency on the phospholipids of the photoreceptor membranes of rat retina. Archives of Biochemistry and Biophysics 151, 270276.CrossRefGoogle Scholar
Anderson, RE, O'Brien, PJ, Weigand, RD, Koutz, CA & Stinson, AM (1992) Conservation of docosahexaenoic acid in the retina. In Advances in Experimental Medical Biology. vol. 318, Neurobiology of Essential Fatty Acids pp. 285294 [Bazan, NG, Murphy, MG and Toffano, G, editors]. New York and London: Plenum Press.Google Scholar
Arisaka, M, Arisaka, O & Yamashiro, Y (1991) Fatty acid and prostaglandin metabolism in children with diabetes mellitus. II. The effect of evening primrose oil supplementation on serum fatty acid and plasma prostaglandin levels. Prostaglandins, Leukotrienes and Essential Fatty Acids 43, 197201.Google Scholar
Barker, DJ (1997) Maternal nutrition, fetal nutrition, and disease in later life. Nutrition 13, 807813.Google Scholar
Brenner, RR (1981) Nutritional and hormonal factors influencing desaturation of essential fatty acids. Progress in Lipid Research 20, 4147.CrossRefGoogle ScholarPubMed
British Nutrition Foundation (1992) Unsaturated fatty acids, thrombogenesis and fibrinolysis. In Unsaturated Fatty Acids: Nutritional and Physiological Significance. Report of the Nutrition Foundation's Task Force, pp. 92111. London: Chapman & Hall.CrossRefGoogle Scholar
Burr, ML, Fehily, AM, Gilbert, JF, Rogers, S, Holliday, RM, Sweetnam, PM, Elwood, PC & Deadman, NM (1989) Effects of changes in fat, fish, and fibre intakes on death and myocardial re-infarction trial (DART). Lancet ii, 757761.CrossRefGoogle Scholar
Caprio, S, Wong, S, Alberti, KG & King, G (1997) Cardiovascular complications of diabetes. Diabetologia 40, Suppl. 3, B78B82.CrossRefGoogle ScholarPubMed
Christine, M, Albert, CM, Hennekens, CH, O'Donnell, CJ, Ajani, UJ, Carey, VJ, Willett, WC, Ruskin, JN & Manson, JE (1998) Fish consumption and risk of sudden cardiac death. Journal of the American Medical Association 279, 2328.Google Scholar
Crawford, MA (1999) The placental delivery of arachidonic and docosahexaenoic acids: implications for the lipid nutrition of the preterm infant. American Journal of Clinical Nutrition (In the Press).Google Scholar
Crawford, MA, Costeloe, K, Doyle, W, Leighfield, MJ, Lennon, EA & Meadows, N (1990) Potential diagnostic value of the umbilical artery as a definition of neural fatty acid status of the fetus during its growth. Biochemical Society Transactions 18, 761766.CrossRefGoogle ScholarPubMed
Crawford, MA, Costeloe, K, Ghebremeskel, K & Phylactos, AC (1997) Are deficits of arachidonic and docosahexaenoic acids responsible for the neural and vascular complications of preterm babies?. American Journal of Clinical Nutrition 66, 1032S1041S.CrossRefGoogle ScholarPubMed
Crawford, MA, Costeloe, K, Ghebremeskel, K & Phylactos, A (1998) The inadequacy of the essential fatty acid content of present preterm feeds. European Journal of Pediatrics 157, Suppl. 1, S23S27.CrossRefGoogle ScholarPubMed
Crawford, MA, Hassam, AG & Rivers, JPW (1978) Vulnerability of the artery during growth. Post Graduate Medical Journal 54, 149153.Google Scholar
Crawford, MA, Hassam, AG, Williams, G & Whitehouse, WL (1976) Essential fatty acids and fetal brain growth. Lancet i, 452453.CrossRefGoogle Scholar
Dally, A (1998) Thalidomide: was the tragedy preventable?. Lancet 351, 11971199.Google Scholar
Fiennes, RNT-W, Sinclair, AJ & Crawford, MA (1973) Essential fatty acid studies in primates: linolenic acid requirements of Capuchins. Journal of Medical Primatology 2, 155169.CrossRefGoogle ScholarPubMed
Folch, J, Lees, M & Sloane-Stanley, GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. Journal of Biological Chemistry 226, 497509.CrossRefGoogle ScholarPubMed
Freyburger, G, Gin, H, Heape, A, Juguelin, H, Boisseau, MR & Cassagne, C (1989) Phospholipid and fatty acid composition of erythrocytes in type I and type II diabetes. Metabolism 38, 673678.CrossRefGoogle ScholarPubMed
Fulesdi, B, Limburg, M, Bereczki, D, Michels, RP, Neuwirth, G, Legemate, D, Valikovics, A & Csiba, L (1997) Impairment of cerebrovascular reactivity in long-term type 1 diabetes. Diabetes 46, 18401845.CrossRefGoogle ScholarPubMed
Gali, C & Socini, A (1983) Dietary lipids in pre- and post-natal development. In Dietary Fats and Health, vol. 16, pp. 278301 [Perkins, EG and Visek, WJ, editors]. Chicago, IL: American Oil Chemists' Society.Google Scholar
Ghebremeskel, K, Leighfield, MJ, Leaf, A, Costeloe, KL & Crawford, MA (1995) Fatty acid composition of plasma and red cell phospholipids of preterm babies fed on breast milk and formulae. European Journal of Pediatrics 154, 4652.CrossRefGoogle ScholarPubMed
Ghebremeskel, K, Thomas, B, Min, Y, Stacey, F, Koukkou, E, Lowy, C, Erskine, K, Crawford, MA & Offley-Shore, B (1997) Fatty acids in pregnant women and neonates: implications for pre and post-natal development. Prostaglandins, Leukotrienes and Essential Fatty Acids 57, M26.Google Scholar
Hornstra, G, Al, M, Houwelingen, AC & Foreman-van Drongelen, MHP (1995) Essential fatty acids in pregnancy and early human development. European Journal of Obstetric and Gynaecological Reproductive Biology 61, 5762.Google Scholar
Holman, RT (1970) Biochemical activities of and requirement for polyunsaturated fatty acids. Progress in the Chemistry of Fats and Lipids 9, 607687.Google Scholar
Holman, RT, Johnson, SB & Hatch, TF (1982) A case of human linolenic acid deficiency involving neurological abnormalities. American Journal of Nutrition 35, 617623.Google ScholarPubMed
Holman, RT, Johnson, SB & Ogburn, PL (1991) Deficiency of essential fatty acids and membrane fluidity during pregnancy and lactation. Proceedings of the National Academy of Sciences USA 88, 48354839.CrossRefGoogle ScholarPubMed
Keys, A (1980) Seven Countries: A Multivariate Analysis of Death and Coronary Heart Disease. London: Harvard University Press.Google Scholar
Keys, A (1997) Coronary heart disease in seven countries: 1970. Nutrition 13, 250252.CrossRefGoogle ScholarPubMed
Koukkou, E, Lowy, C & Poston, L (1998) Young offspring of normal and diabetic rats fed saturated fats in pregnancy exhibit vascular dysfunction Circulation (In the Press).CrossRefGoogle Scholar
Kuhn, DC, Crawford, MA, Stuart, MJ, Botti, JJ & Demers, LM (1990) Alterations in transfer and lipid distribution of arachidonic acid in placentas of diabetic pregnancies. Diabetes 39, 914918.CrossRefGoogle ScholarPubMed
Lands, WEM (1991) Biosynthesis of prostaglandins. Annual Review of Nutrition 11, 41–6.Google Scholar
Lauer, RM, Clarke, WR & Rames, LK (1978) Blood pressure and its significance in childhood. Post Graduate Medical Journal 54, 206210.CrossRefGoogle ScholarPubMed
Louw, ME, du Plessis, JP & Van den Berg, AS (1969) Intercorrelation study of dietary and biochemical data from school children in the Pretoria area. South African Medical Journal 43, 15161518.Google Scholar
Newman, WP, Freedman, DS, Voors, AW, Gard, PD, Srinivasan, SR, Cresanta, JL, Williamson, GD, Webber, LS & Berensen, GS (1986) Relation of serum lipoprotein levels and systolic blood pressure to early atherosclerosis: the Bogalusa Heart Study. New England Journal of Medicine 314, 138144.CrossRefGoogle ScholarPubMed
O'Neil, CE, Nicklas, TA, Myers, L, Johnson, CC & Berenson, GS (1997) Cardiovascular risk factors and behavior lifestyles of young women: implications from findings of Bogalusa Heart Study. American Journal of Medical Sciences 314, 385395.Google ScholarPubMed
Osborne, G (1967) Stages in Development of Coronary Artery Disease Observed From 1,500 Young Subjects. Paris: Editions du Centre National de la Recherché Scientifique.Google Scholar
Pesonen, E, Noris, R, Hirvonen, J, Karkola, K, Kuusela, V, Laaksonen, H, Mottonen, M, Nikkari, T, Raekallioet, J & Viikari, J (1990) Intimal thickening in the coronary arteries of infants and children as an indicator of risk factors for coronary heart disease. European Heart Journal 11, Suppl. E, 5360.Google Scholar
Ruyle, M, Connor, WE, Anderson, GJ & Lowensohn, RL (1990) Placental transfer of essential fatty acids in humans: venous-arterial difference for docosahexaenoic acid in fetal umbilical erythrocytes. Proceedings of the National Academy of Sciences USA 87, 79027905.CrossRefGoogle ScholarPubMed
Sinclair, AJ (1975) Long chain polyunsaturated fatty acids in the mammalian brain. Proceedings of the Nutrition Society 34, 287291.CrossRefGoogle ScholarPubMed
Sprecher, H (1986) The metabolism of (n-3) and (n-6) fatty acids and their oxygenation by platelet cyclooxygenase and lipooxygenase. Progress in Lipid Research 25, 1928.CrossRefGoogle Scholar
Sprecher, H (1992) Interconversions between 20- and 22-carbon n-3 and n-6 fatty acids via 4-desaturase independent pathways. In Essential Fatty Acids and Eicosanoids, pp. 1822 [Sinclair, AJ and Gibson, R, editors]. Champaign, IL: American Oil Chemists' Society.Google Scholar
Suzuki, H, Manabe, S, Wada, O & Crawford, MA (1997) Rapid incorporation of docosahexaenoic acid from dietary sources into brain microsomal, synaptosomal and mitochondrial membranes in adult mice. International Journal of Vitamin and Nutrition Research 67, 272278.Google Scholar
Xiao, YF, Gomez, AM, Morgan, JP, Lederer, WJ & Leaf, A (1997) Suppression of voltage-gated L-type Ca2+ currents by polyunsaturated fatty acids in adult and neonatal rat ventricular myocytes. Proceedings of the National Academy of Sciences USA 94, 41824187.Google Scholar