Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-10T19:44:28.879Z Has data issue: false hasContentIssue false

Nutrient partitioning during pregnancy: adverse gestational outcome in overnourished adolescent dams

Published online by Cambridge University Press:  28 February 2007

Jacqueline M. Wallace*
Affiliation:
Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen AB21 9SB, UK
*
*Corresponding author: Dr Jacqueline M. Wallace, fax +44 (0)1224 716622, email jwra@rri.sari.ac.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.

Appropriate nutrient partitioning between the maternal body and gravid uterus is essential for optimum fetal growth and neonatal survival, and in adult sheep nutrient partitioning during pregnancy generally favours the conceptus at the expense of the dam. However, recent studies using an overnourished adolescent sheep model demonstrate that the hierarchy of nutrient partitioning during pregnancy can be dramatically altered in young growing females. Overnourishing the adolescent dams to promote rapid maternal growth throughout pregnancy results in a major restriction in placental mass and leads to a significant decrease in birth weight relative to moderately-fed adolescents of equivalent gynaecological age. High maternal feed intakes are also associated with an increased incidence of non-infectious spontaneous abortion, a reduction in gestation length and colostrum production, and a higher incidence of neonatal mortality. The present paper examines the putative role of a variety of endocrine regulators of nutrient partitioning in this unusual model system, where the dam is overnourished while the stunted placenta restricts nutrient supply to the fetus. The central role of nutritionally-mediated alterations in placental growth and development in setting the subsequent pattern of nutrient partitioning between the maternal body, placenta and fetus is examined, and critical periods of sensitivity to alterations in maternal nutritional status are defined. Finally, the consequences of this form of inappropriate nutrient partitioning on the growth and development of the fetus and neonate are described with particular emphasis on the reproductive axis.

Type
Clinical Nutrition and Metabolism Group Symposium on ‘Clinical nutrition in childhood’
Copyright
Copyright © The Nutrition Society 2000

References

Alexander, G & Williams, D (1971) Heat stress and development of the conceptus in domestic sheep. Journal of Agricultural Science, Cambridge 76, 5372.CrossRefGoogle Scholar
Anthony, RV, Pratt, SL, Liang, R & Holland, MD (1995) Placental–fetal hormonal interactions: impact on fetal growth. Journal of Animal Science 73, 18611871.CrossRefGoogle ScholarPubMed
Barcroft, J (1946) Researches on Prenatal Life. Oxford: Blackwell Scientific Publications.Google Scholar
Barcroft, J & Kennedy, JA (1939) The distribution of blood flow between the foetus and placenta in sheep. Journal of Physiology 95, 173186.CrossRefGoogle Scholar
Barker, DJP (1995) Fetal origins of coronary heart disease. British Medical Journal 311, 171174.CrossRefGoogle ScholarPubMed
Barker, DJP, Bull, AR, Osmond, C & Simmonds, SJ (1990) Fetal and placental size and risk of hypertension in adult life. British Medical Journal 301, 259262.CrossRefGoogle ScholarPubMed
Bauer, MK, Harding, JE, Bassett, NS, Breier, BH, Oliver, MH, Gallaher, BH, Evans, PC, Woodall, SM & Gluckman, PD (1998) Fetal growth and placental function. Molecular and Cellular Endocrinology 140, 115120.CrossRefGoogle ScholarPubMed
Bauman, DE & Currie, WB (1980) Partitioning of nutrients during pregnancy and lactation: a review of mechanisms involving homeostasis and homeorhesis. Journal of Dairy Science 63, 15141529.CrossRefGoogle ScholarPubMed
Bell, AW (1984) Factors controlling placental and foetal growth and their effects on future production. In Reproduction in Sheep, pp. 144152 [Lindsay, DR and Pearce, PT, editors]. Canberra: Australian Academy of Science.Google Scholar
Bell, AW (1992) Foetal growth and its influence on postnatal growth and development. In The Control of Fat and Lean Deposition, pp. 111127 [Boormann, KN, Buttery, PJ and Lindsay, DB, editors]. Oxford: Butterworth-Heinemann Ltd.CrossRefGoogle Scholar
Bell, AW (1993) Pregnancy and fetal metabolism. In Quantitative Aspects of Ruminant Digestion and Metabolism, pp. 405431 [Forbes, JM and France, J, editors]. Wallingford, Oxon: CAB International.Google Scholar
Bell, AW & Bauman, DE (1994) Animal models for the study of adipose regulation in pregnancy and lactation. In Nutrient Regulation during Pregnancy, Lactation, and Infant Growth, pp. 184 [Allen, L, King, J and Lonnerdal, B, editors]. New York: Plenum Press.Google Scholar
Bell, AW & Bauman, DE (1997) Adaptations of glucose metabolism during pregnancy and lactation. Journal of Mammary Gland Biology and Neoplasia 2, 265278.CrossRefGoogle ScholarPubMed
Bell, AW, Hay WW, Jr & Ehrhardt, RA (1999) Placental transport of nutrients and its implications for fetal growth. Journal of Reproduction and Fertility, Suppl. 54, 401410.Google ScholarPubMed
Brown, CA & Thorburn, GD (1989) Endocrine control of fetal growth. Biology of the Neonate 55, 331346.CrossRefGoogle Scholar
Carter, AM & Myatt, L (1995) Control of placental blood flow: Workshop report. Reproduction, Fertility and Development 7, 14011406.CrossRefGoogle Scholar
Da Silva, P, Aitken, RP, Brooks, AN, Rhind, SM & Wallace, JM (1998) Perturbed pituitary gonadotrophin gene expression and gonadal development in growth restricted fetal lambs at day 128 of gestation. Journal of Reproduction and Fertility Abstract Series 22, 10.Google Scholar
Da Silva, P, Aitken, RP, Rhind, SM & Wallace, JM (1999) Placentally-mediated fetal growth restriction influences the onset of puberty in male but not in female lambs. Journal of Reproduction and Fertility Abstract Series 23, 24.Google Scholar
Dodic, M, May, CN, Wintour, EM & Coghlan, JP (1998) An early prenatal exposure to excess glucocorticoid leads to hypertensive offspring in sheep. Clinical Science 94, 149155.CrossRefGoogle ScholarPubMed
Ehrhardt, RA & Bell, AW (1995) Growth and metabolism of the ovine placenta during mid-gestation. Placenta 16, 727741.CrossRefGoogle ScholarPubMed
Flint, DJ, Sinnett-Smith, PA, Clegg, RA & Vernon, RG (1979) Role of insulin receptors in the changing metabolism of adipose tissue during pregnancy and lactation in the rat. Biochemistry Journal 182, 421427.CrossRefGoogle ScholarPubMed
Fraser, AM, Brockert, JE & Ward, RH (1995) Association of young maternal age with adverse reproductive outcomes. New England Journal of Medicine 332, 11131117.CrossRefGoogle ScholarPubMed
Frisancho, AR, Matos, J, Leonard, WR & Yarouch, LA (1985) Developmental and nutritional determinants of pregnancy outcome among teenagers. American Journal of Physical Anthropology 66, 247261.CrossRefGoogle ScholarPubMed
Giudice, LC (1994) Growth factors and growth modulators in human endometrium: Their potential relevance to reproductive medicine. Fertility and Sterility 61, 117.CrossRefGoogle ScholarPubMed
Grizard, J, Dardevet, D, Papet, I, Mosoni, L, Mirand, PP, Attaix, D, Tauveron, I, Bonin, D & Arnal, M (1995) Nutrient regulation of skeletal muscle protein metabolism in animals. The involvement of hormones and substrates. Nutrition Research Reviews 8, 6791.CrossRefGoogle ScholarPubMed
Guesnet, M, Massoud, MJ & Demarne, Y (1991) Regulation of adipose tissue metabolism during pregnancy and lactation in the ewe: the role of insulin. Journal of Animal Science 69, 20572065.CrossRefGoogle ScholarPubMed
Harding, JE & Johnston, BM (1995) Nutrition and fetal growth. Reproduction, Fertility and Development 7, 539547.CrossRefGoogle ScholarPubMed
Harding, JE, Liu, L, Evans, PC & Gluckman, PD (1994) Insulin-like growth factor 1 alters feto-placental protein and carbohydrate metabolism in fetal sheep. Endocrinology 134, 15091514.CrossRefGoogle ScholarPubMed
Hartwich, KM, Walker, SK, Owens, JA & Seamark, RF (1995) Progesterone supplementation in the ewe alters cell allocation to the inner cell mass. Proceedings of the Australian Society of Medical Research 26,128 Abstr.Google Scholar
Heasman, L, Clarke, L, Firth, K, Stephenson, T & Symonds, ME (1998) Influence of restricted maternal nutrition in early to mid gestation on placental and fetal development at term in sheep. Paediatric Research 44, 546551.CrossRefGoogle ScholarPubMed
Hoggard, N, Hunter, L, Duncan, JS, Williams, LM, Trayhurn, P & Mercer, JG (1997) Leptin and leptin receptor mRNA and protein expression in the murine fetus and placenta. Proceedings of the National Academy of Sciences USA 94, 1107311078.CrossRefGoogle ScholarPubMed
Holemans, K, Aerts, L & Van Assche, FA (1998) Fetal growth and long-term consequences in animal models of growth retardation. European Journal of Obstetrics and Gynecology and Reproductive Biology 81, 149156.CrossRefGoogle ScholarPubMed
Hough, GM, McDowell, GH, Annison, EF & Williams, AJ (1985) Glucose metabolism in hindlimb muscle of pregnant and lactating ewes. Proceedings of the Nutrition Society of Australia 10, 97.Google Scholar
Houseknecht, KL, Bauman, DE, Vernon, RG, Byatt, JC & Collier, RJ (1996) Insulin-like growth factors-I and II, somatotropin, prolactin and placental lactogen are not acute effectors of lipolysis in ruminants. Domestic Animal Endocrinology 13, 239249.CrossRefGoogle Scholar
Jenkinson, CMC, Min, SH, Mackenzie, DDS, McCutcheon, SN, Breier, BH & Gluckman, PD (1999) Placental development and fetal growth in growth hormone-treated ewes. Growth Hormone and IGF Research 9, 1117.CrossRefGoogle ScholarPubMed
Johnsson, ID & Hart, IC (1985) Pre-pubertal mammogenesis in the sheep 1. The effects of level of nutrition on growth and mammary development in female lambs. Animal Production 41, 323332.Google Scholar
Johnsson, ID & Obst, JM (1984) The effects of level of nutrition before and after 8 months of age on subsequent milk and calf production of beef heifers over three lactations. Animal Production 38, 5768.Google Scholar
Kelly, RW (1992) Nutrition and placental development. Proceedings of the Nutrition Society of Australia 17, 203211.Google Scholar
Kleemann, DO, Walker, SK & Seamark, RF (1994) Enhanced fetal growth in sheep administered progesterone during the first three days of pregnancy. Journal of Reproduction and Fertility 102, 411417.CrossRefGoogle ScholarPubMed
Lacroix, MC, Servely, JL & Kann, G (1995) IGF-I and IGF-II receptors in the sheep placenta: evolution during the course of pregnancy. Journal of Endocrinology 144, 179191.CrossRefGoogle ScholarPubMed
Langley-Evans, SC, Gardner, DS & Welham, SJM (1998) Intrauterine programming of cardiovascular disease by maternal nutritional status. Nutrition 14, 3947.CrossRefGoogle ScholarPubMed
Lea, RG, Hannah, L, Blades, J, Howe, D & Hoggard, N (1998) Placental leptin in normal and abnormal pregnancies. Journal of Reproduction and Fertility Abstract Series 21, 21.Google Scholar
Lenders, CM, Hediger, ML, Scholl, TO, Khoo, CS, Slap, GB & Stallings, VA (1997) Gestational age and infant size at birth are associated with dietary sugar intake among pregnant adolescents Journal of Nutrition 127, 11131117.CrossRefGoogle ScholarPubMed
Lok, F, Owens, JA, Mundy, L, Robinson, JS & Owens, PC (1996) Insulin-like growth factor 1 promotes growth selectively in fetal sheep in late gestation. American Journal of Physiology 270, R1148R1155.Google ScholarPubMed
McAnarney, ER (1987) Young maternal age and adverse neonatal outcome. American Journal of Diseases of Children 141, 10531059.Google ScholarPubMed
McMillen, IC, Phillips, ID, Ross, JT, Robinson, JS & Owens, JA (1995) Chronic stress – the key to parturition. Reproduction, Fertility and Development 7, 499507.CrossRefGoogle ScholarPubMed
Mellor, DJ (1983) Nutritional and placental determinants of foetal growth rate in sheep and consequences for the newborn lamb British Veterinary Journal 139, 307324.CrossRefGoogle ScholarPubMed
Mellor, DJ (1987) Nutritional effects on the fetus and mammary gland during pregnancy. Proceedings of the Nutrition Society 46, 249257.CrossRefGoogle ScholarPubMed
Molina, RD, Meschia, G & Wilkening, RB (1990) Uterine blood flow, oxygen and glucose uptakes at mid-gestation in the sheep. Proceedings of the Society for Experimental Biology and Medicine 195, 379385.CrossRefGoogle ScholarPubMed
Oddy, VH, Gooden, JM, Hough, GM, Teleni, E & Annison, EF (1985) Partitioning of nutrients in Merino ewes II. Glucose utilisation by skeletal muscle, the pregnant uterus and the lactating mammary gland in relation to whole body glucose utilisation. Australian Journal of Biological Science 38, 95108.CrossRefGoogle Scholar
Oddy, VH & Holst, PJ (1991) Maternal-foetal adaptation to mid pregnancy feed restriction in single-bearing ewes. Australian Journal of Agricultural Research 42, 969978.CrossRefGoogle Scholar
Olausson, PO, Cnattingius, S & Haglund, B (1999) Teenage pregnancies and risk of late fetal death and infant mortality. British Journal of Obstetrics and Gynaecology 106, 116121.CrossRefGoogle ScholarPubMed
Oliver, MH, Bloomfield, FH, Harding, JE, Breier, BH, Bassett, NS & Gluckman, PD (1999) The maternal, fetal and postnatal somatotrophic axes in intrauterine growth retardation. Biochemical Society Transactions 27, 6973.CrossRefGoogle ScholarPubMed
Oliver, MH, Harding, JE, Breier, BH & Gluckman, PD (1996) Fetal insulin-like growth factor (IGF)-I and IGF-II are regulated differently by glucose or insulin in the sheep fetus. Reproduction, Fertility and Development 8, 167172.CrossRefGoogle ScholarPubMed
Owens, JA (1991) Endocrine and substrate control of fetal growth: placental and maternal influences and insulin-like growth factors. Reproduction, Fertility and Development 3, 501517.CrossRefGoogle ScholarPubMed
Owens, JA, Kind, KL, Carbone, F, Robinson, JS & Owens, PC (1994) Circulating insulin-like growth factors-I and -II and substrates in fetal sheep following restriction of placental growth. Journal of Endocrinology 140, 513.CrossRefGoogle ScholarPubMed
Owens, JA, Owens, PC & Robinson, JS (1995) Experimental restriction of fetal growth. In Fetus and Neonate, Physiology and Clinical Applications, pp. 139175 [Hanson, MA, Spencer, JAD and Rodeck, CH, editors]. Cambridge: Cambridge University Press.Google Scholar
Palmer, RM, Thompson, MG, Millet, C, Thom, A, Aitken, RP & Wallace, JM (1998) Growth and metabolism of fetal and maternal muscles of adolescent sheep on adequate or high feed intakes: possible role of protein kinase C-α in fetal muscle growth. British Journal of Nutrition 79, 351357.CrossRefGoogle ScholarPubMed
Parr, RA, Williams, AH, Campbell, IP, Witcome, GF & Roberts, AM (1986) Low nutrition of ewes in early pregnancy and the residual effect on the offspring. Journal of Agricultural Science, Cambridge 106, 8187.CrossRefGoogle Scholar
Rattray, PV, Garrett, WN, East, NE & Hinman, N (1974) Growth development and composition of the ovine mammary gland during pregnancy. Journal of Animal Science 38, 613626.CrossRefGoogle ScholarPubMed
Reynolds, LP & Redmer, DA (1995) Utero-placental vascular development and placental function. Journal of Animal Science 73, 18391851.CrossRefGoogle ScholarPubMed
Reynolds, TS, Stevenson, KR & Wathes, DC (1997) Pregnancy-specific alterations in the expression of the insulin-like growth factor system during early placental development in the ewe. Endocrinology 138, 886897.CrossRefGoogle ScholarPubMed
Reynolds, TS, Wathes, DC, Aitken, RP & Wallace, JM (2000) Effect of maternal nutrition on components of the insulin-like growth factor (IGF) system and placental growth. Journal of Reproduction and Fertility (In the Press).Google Scholar
Robinson, JJ (1983) Nutrition of the pregnant ewe. In Sheep Production, pp. 111131 [Haresign, W, editor]. London: Butterworths.Google Scholar
Robinson, JJ, McDonald, I, McHattie, I & Pennie, K (1978) Studies on reproduction in prolific ewes 4. Sequential changes in the maternal body during pregnancy. Journal of Agricultural Science, Cambridge 91, 291304.CrossRefGoogle Scholar
Robinson, JJ, Sinclair, KD & McEvoy, TG (1999) Nutritional effects on foetal growth. Animal Science 68, 315331.CrossRefGoogle Scholar
Rush, D (1986) Nutrition in the preparation for pregnancy. In Prepregnancy Care: A Manual for Practice, pp. 113139 [Chamberlain, G and Lumley, J, editors]. Chichester, West Sussex: John Wiley and Sons Ltd.Google Scholar
Samad, AR & Ford, EJH (1981) The effects of progesterone on glucose and lactate metabolism in ovariectomised sheep. Quarterly Journal of Experimental Physiology 66, 7380.CrossRefGoogle Scholar
Schneider, H (1996) Ontogenic changes in the nutritive function of the placenta. Placenta 17, 1526.CrossRefGoogle ScholarPubMed
Scholl, TO & Hediger, ML (1993) A review of the epidemiology of nutrition and adolescent pregnancy: maternal growth during pregnancy and its effect on the fetus. Journal of the American College of Nutrition 12, 101107.CrossRefGoogle ScholarPubMed
Scottish Needs Assessment Programme (1994) Teenage pregnancy in Scotland- report. Scottish Forum for Public Health Medicine, pp. 34.Glasgow: Scottish Forum for Public Health Medicine.Google Scholar
Steyn, C, Koser, F, Hawkins, P, Saito, T, Ozaki, T, Noakes, D & Hanson, M (2000) Effect of mild undernutrition in early gestation on fetal villous density in sheep. Placenta (In the Press).Google Scholar
Thissen, JP, Ketelslegers, JM & Underwood, LE (1994) Nutritional regulation of the insulin-like growth factors. Endocrine Reviews 15, 80101.Google ScholarPubMed
Torry, DS & Torry, RJ (1997) Angiogenesis and the expression of vascular endothelial growth factor in endometrium and placenta. American Journal of Reproductive Immunology 37, 2129.CrossRefGoogle ScholarPubMed
Umberger, SH, Goode, L, Caruolo, EV, Harvey, RW, Britt, JH & Linnerud, AC (1985) Effects of accelerated growth during rearing on reproduction and lactation in ewes lambing at 13 to 15 months of age. Theriogenology 23, 555564.CrossRefGoogle ScholarPubMed
Vatnick, I, Schoknecht, PA, Darrigrand, R & Bell, AW (1991) Growth and metabolism of the placenta after unilateral fetectomy in twin pregnant ewes. Journal of Developmental Physiology 15, 351356.Google ScholarPubMed
Vernon, RG, Clegg, RA & Flint, DJ (1981) Metabolism of sheep adipose tissue during pregnancy and lactation. Biochemistry Journal 200, 307314.CrossRefGoogle ScholarPubMed
Vernon, RG & Finley, E (1986) Endocrine control of lipogenesis on adipose tissue from lactating sheep. Biochemical Society Transactions 14, 635636.CrossRefGoogle Scholar
Vincent, IC, Williams, HLI & Hill, R (1985) The influence of a low-nutrient intake after mating on gestation and perinatal survival of lambs. British Veterinary Journal 141, 611617.CrossRefGoogle ScholarPubMed
Wallace, JM, Aitken, RP & Cheyne, MA (1994) Effect of post-ovulation nutritional status in ewes on early conceptus survival and growth in vivo and luteotrophic protein secretion in vitro. Reproduction, Fertility and Development 6, 253259.CrossRefGoogle ScholarPubMed
Wallace, JM, Aitken, RP & Cheyne, MA (1996) Nutrient partitioning and fetal growth in rapidly growing adolescent ewes. Journal of Reproduction and Fertility 107, 183190.CrossRefGoogle ScholarPubMed
Wallace, JM, Aitken, RP, Cheyne, MA & Humblot, P (1997a) Pregnancy-specific protein B and progesterone concentrations in relation to nutritional regimen, placental mass and pregnancy outcome in growing adolescent ewes carrying singleton fetuses. Journal of Reproduction and Fertility 109, 5358.CrossRefGoogle ScholarPubMed
Wallace, JM, Bourke, DA & Aitken, RP (1999a) Nutrition and fetal growth: paradoxical effects in the overnourished adolescent sheep. Journal of Reproduction and Fertility, Suppl. 54, 385399.Google ScholarPubMed
Wallace, JM, Bourke, DA, Aitken, RP & Cruickshank, MA (1999b) Switching maternal nutrient intake at the end of the first trimester has profound effects on placental development and fetal growth in adolescent sheep carrying singleton fetuses. Biology of Reproduction 61, 101110.CrossRefGoogle ScholarPubMed
Wallace, JM, Bourke, DA & Aitken, RP, Da, Silva P & Cruickshank, MA (1998) Influence of progesterone supplementation during the first trimester on pregnancy outcome in overnourished adolescent ewes. Journal of Reproduction and Fertility Abstract Series 22, 23.Google Scholar
Wallace, JM, Bourke, DA, Aitken, RP, Palmer, RM, Da Silva, P & Cruickshank, MA (2000) Relationship between nutritionally-mediated placental growth restriction and fetal growth, body composition and endocrine status during late gestation in adolescent sheep. Placenta 21,(In the Press).CrossRefGoogle ScholarPubMed
Wallace, JM, Da, Silva P, Aitken, RP & Cruickshank, MA (1997b) Maternal endocrine status in relation to pregnancy outcome in rapidly growing adolescent sheep. Journal of Endocrinology 155, 359368.CrossRefGoogle ScholarPubMed
Wallace, LR (1948a) The growth of lambs before and after birth in relation to the level of nutrition. Journal of Agricultural Science, Cambridge 38, 243300.CrossRefGoogle Scholar
Wallace, LR (1948b) The growth of lambs before and after birth in relation to the level of nutrition. Journal of Agricultural Science, Cambridge 38, 367398.CrossRefGoogle Scholar
Wathes, DC, Reynolds, TS, Robinson, RS & Stevenson, KR (1998) Role of insulin-like growth factor system in uterine function and placental development in ruminants. Journal of Dairy Science 81, 17781789.CrossRefGoogle ScholarPubMed
Wilson, V, Dandrea, J, Stephenson, T, Webb, R & Symonds, ME (2000) The influence of maternal nutrient restriction between early to mid gestation on placental weight and leptin abundance. Proceedings of the Nutrition Society 59, OCAGoogle Scholar