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REVIEW

Prenatal programming of postnatal productivity and health of livestock: a brief review

A. W. Bell
+ Author Affiliations
- Author Affiliations

Department of Animal Science, Cornell University, Ithaca, NY 14853-4801, USA. Email: awb6@cornell.edu

Australian Journal of Experimental Agriculture 46(7) 725-732 https://doi.org/10.1071/EA06006
Submitted: 30 December 2005  Accepted: 15 March 2006   Published: 8 June 2006

Abstract

Human epidemiological evidence has suggested that metabolic perturbations during fetal life may increase predisposition to cardiovascular disease, type 2 diabetes and obesity in later life. A growing number of controlled experiments on sheep and other large animal species are adding to the already large body of experimental evidence from rat studies in supporting the ‘fetal origins’ hypothesis. Of particular practical relevance are findings that maternal undernutrition in late pregnancy can predispose lambs to glucose intolerance and increased adiposity in early adulthood. This effect may be exacerbated by high energy intakes and limited capacity for muscle growth in undernourished or growth-retarded lambs during early postnatal life. Recent Australian studies have demonstrated the effects of prenatal nutrition on postnatal growth and meat production in beef cattle, and on quantity and quality of wool production in sheep.


References


Alexander G (1974) Birth weight of lambs: influences and consequences. In ‘Size at birth’. (Eds K Elliott, J Knight) pp. 215–239. (Elsevier: Amsterdam)

Barker DJP (2004) The developmental origins of chronic adult disease. Acta Paediatrica Supplement 446, 26–33. open url image1

Bell AW (1992) Foetal growth and its influence on postnatal growth and development. In ‘The control of fat and lean deposition’. (Eds PJ Buttery, KN Boorman, DB Lindsay) pp. 111–127. (Butterworth-Heineman: Oxford, UK)

Brennan KA, Olson DM, Symonds ME (2006) Maternal nutrient restriction alters renal development and blood pressure regulation of the offspring. The Proceedings of the Nutrition Society 65, 116–124.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Clarke L, Firth K, Heasman L, Juniper DT, Budge H , et al. (2000) Influence of size at birth on growth and glucose homeostasis in twin lambs during juvenile life. Reproduction, Fertility and Development 12, 69–73.
Crossref | GoogleScholarGoogle Scholar | open url image1

Clarke KA, Ward JW, Forhead AJ, Giussani DA, Fowden AL (2002) Regulation of 11β-hydroxysteroid dehydrogenase type 2 activity in ovine placenta by fetal cortisol. Journal of Endocrinology 172, 527–534.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Cronjé P (2003) Foetal programming of immune competence. Australian Journal of Experimental Agriculture 43, 1427–1430.
Crossref | GoogleScholarGoogle Scholar | open url image1

Da Silva P, Aitken RP, Rhind SM, Racey PA, Wallace JM (2001) Influence of placentally mediated fetal growth restriction on the onset of puberty in male and female lambs. Reproduction 122, 375–383.
Crossref | PubMed |
open url image1

Da Silva P, Aitken RP, Rhind SM, Racey PA, Wallace JM (2002) Impact of maternal nutrition during pregnancy on pituitary gonadotrophin gene expression and ovarian development in growth-restricted and normally grown late gestation sheep fetuses. Reproduction 123, 769–777.
Crossref | PubMed |
open url image1

Da Silva-Buttkus P, van den Hurk R, te Velde ER, Taverne MA (2003) Ovarian development in intrauterine growth-retarded and normally developed piglets originating from the same litter. Reproduction 126, 249–258.
Crossref | PubMed |
open url image1

Edwards LJ, Symonds ME, Warnes KE, Owens JA, Butler TG , et al. (2001) Responses of the fetal pituitary–adrenal axis to acute and chronic hypoglycemia during late gestation in the sheep. Endocrinology 142, 1778–1785.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ehrhardt RA, Bell AW, Boisclair YR (2002) Spatial and developmental regulation of leptin in fetal sheep. The American Journal of Physiology 282, R1628–R1635. open url image1

Ehrhardt RA, Greenwood PL, Bell AW, Boisclair YR (2003) Plasma leptin is regulated predominantly by nutrition in preruminant lambs. Journal of Nutrition 133, 4196–4201.
PubMed |
open url image1

Eriksson JG, Forsen T (2002) Unravelling the fetal origins hypothesis. Lancet 360, 2072.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Eriksson JG, Forsen T, Tuomilehto J, Jaddoe VW, Osmond C , et al. (2002) Effects of size at birth and childhood growth on the insulin resistance syndrome in elderly individuals. Diabetologia 45, 342–348.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Everitt GC (1968) Prenatal development of uniparous animals, with particular reference to the influence of maternal nutrition in sheep. In ‘Growth and development of mammals’. (Eds GA Lodge, GE Lamming). pp. 131–157. (Butterworths: London)

Fahey AJ, Brameld JM, Parr T, Buttery PJ (2005) The effect of maternal undernutrition before muscle differentiation on the muscle fiber development of the newborn lamb. Journal of Animal Science 83, 2564–2571.
PubMed |
open url image1

Gardner DS, Pearce S, Dandrea J, Walker R, Ramsey MM , et al. (2004) Peri-implantation undernutrition programs blunted angiotensin II evoked baroreflex responses in young adult sheep. Hypertension 43, 1290–1296.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gardner DS, Tingey K, Van Bon BWM, Ozanne SE, Wilson V , et al. (2005) Programming of glucose-insulin metabolism in adult sheep after maternal undernutrition. The American Journal of Physiology 289, R947–R954. open url image1

Gatford KL, Clarke IJ, De Blasio MJ, McMillen IC, Robinson JS , et al. (2002) Perinatal growth and plasma GH profiles in adolescent and adult sheep. Journal of Endocrinology 173, 151–159.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gilbert JS, Lang AL, Grant AR, Nijland MJ (2005) Maternal nutrient restriction in sheep: hypertension, decreased nephron number in offspring at 9 months of age. Journal of Physiology 565, 137–148.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gnanalingham MG, Mostyn A, Symonds ME, Stephenson T (2005) Ontogeny and nutritional programming of adiposity in sheep: potential role of glucocorticoid action and uncoupling protein-2. The American Journal of Physiology 289, R1407–R1415. open url image1

Gopalakrishnan GS, Gardner DS, Rhind SM, Rae MT, Kyle CE , et al. (2004) Programming of adult cardiovascular function after early maternal undernutrition in sheep. The American Journal of Physiology 287, R12–R20.
Crossref |
open url image1

Gopalakrishnan GS, Gardner DS, Dandrea J, Langley-Evans SC, Pearce S , et al. (2005) Influence of maternal pre-pregnancy body composition and diet during early-mid pregnancy on cardiovascular function and nephron number in juvenile sheep. The British Journal of Nutrition 94, 938–947.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Greenwood PL, Bell AW (2003) Consequences of intra-uterine growth retardation for postnatal growth, metabolism and pathophysiology. Reproduction Supplement 61, 195–206. open url image1

Greenwood PL, Hunt AS, Hermanson JW, Bell AW (1998) Effects of birth weight and postnatal nutrition on neonatal sheep: I. Body growth and composition, and some aspects of energetic efficiency. Journal of Animal Science 76, 2354–2367.
PubMed |
open url image1

Greenwood PL, Slepetis RM, Hermanson JW, Bell AW (1999) Intrauterine growth retardation is associated with reduced cell cycle activity, but not myofibre number, in ovine fetal muscle. Reproduction, Fertility and Development 11, 281–291.
Crossref | GoogleScholarGoogle Scholar | open url image1

Greenwood PL, Hunt AS, Hermanson JW, Bell AW (2000) Effects of birth weight and postnatal nutrition on neonatal sheep: II. Skeletal muscle growth and development. Journal of Animal Science 78, 50–61.
PubMed |
open url image1

Greenwood PL, Hunt AS, Slepetis RM, Finnerty KD, Alston C , et al. (2002) Effects of birth weight and postnatal nutrition on neonatal sheep: III. Regulation of energy metabolism. Journal of Animal Science 80, 2850–2861.
PubMed |
open url image1

Greenwood PL, Cafe LM, Hearnshaw H, Hennessy DW (2005) Consequences of nutrition and growth retardation early in life for growth and composition of cattle and eating quality of beef. Recent Advances in Animal Nutrition in Australia 15, 183–195. open url image1

Gunn RG, Sim DA, Hunter EA (1995) Effects of nutrition in utero and in early life on the subsequent lifetime reproductive performance of Scottish Blackface ewes in two management systems. Animal Science (Penicuik, Scotland) 60, 223–230. open url image1

Hawkins P, Steyn C, McGarrigle HHG, Calder NA, Saito T , et al. (2000) Cardiovascular and hypothalamic–pituitary axis development in late gestation fetal sheep and young lambs following modest maternal nutrient restriction in early gestation. Reproduction, Fertility and Development 12, 443–456.
Crossref | GoogleScholarGoogle Scholar | open url image1

Huxley R, Neil A, Collins R (2002) Unravelling the fetal origins hypothesis: is there really an inverse association between birthweight and subsequent blood pressure? Lancet 360, 659–665.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Joseph KS, Kramer MS (1996) Review of the evidence on fetal and early childhood antecedents of adult chronic disease. Epidemiologic Reviews 18, 158–174.
PubMed |
open url image1

Kelly RW, Macleod I, Hynd P, Greeff J (1996) Nutrition during fetal life alters annual wool production and quality in young Merino sheep. Australian Journal of Experimental Agriculture 36, 259–267.
Crossref | GoogleScholarGoogle Scholar | open url image1

Krausgrill DI, Tulloh NM, Shorthose WR, Sharpe K (1999) Effects of weight loss in ewes in early pregnancy on muscles and meat quality of lambs. Journal of Agricultural Science, Cambridge 132, 103–116.
Crossref | GoogleScholarGoogle Scholar | open url image1

Langley-Evans SC (2006) Developmental programming of health and disease. The Proceedings of the Nutrition Society 65, 97–105.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Leon DA, Johansson M, Rasmussen F (2000) Gestational age and growth rate of fetal mass are inversely associated with systolic blood pressure in young adults: an epidemiologic study of 165,136 Swedish men aged 18 years. American Journal of Epidemiology 152, 597–604.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Limesand SW, Hay WW (2003) Adaptation of ovine fetal pancreatic insulin secretion to chronic hypoglycaemia and euglycaemic correction. Journal of Physiology 547, 95–105.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Limesand SW, Jensen J, Hutton JC, Hay WW (2005) Diminished β-cell replication contributes to reduced β-cell mass in fetal sheep with intrauterine growth restriction. The American Journal of Physiology 288, R1297–R1305. open url image1

MacLaughlin SM, Walker SK, Roberts CT, Kleemann DO, McMillen IC (2005) Periconceptual nutrition and the relationship between maternal body weight changes in the periconceptual period and feto-placental growth in the sheep. Journal of Physiology 565, 111–124.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

McMillen IC, Robinson JS (2005) Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiological Reviews 85, 571–633.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

McMillen IC, Muhlhausler BS, Duffield JA, Yuen BS (2004) Prenatal programming of postnatal adiposity: fetal nutrition and the regulation of leptin synthesis and secretion before birth. The Proceedings of the Nutrition Society 63, 405–412.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

McMullen S, Osgerby JC, Thurston LM, Gadd TS, Wood PJ , et al. (2004) Alterations in placental 11β-hydroxysteroid dehydrogenase (11βHSD) activities and fetal cortisol:cortisone ratios induced by nutritional restriction prior to conception and at defined stages of gestation in ewes. Reproduction 127, 717–725.
Crossref | PubMed |
open url image1

Nordby DJ, Field RA, Riley ML, Kercher CJ (1987) Effects of maternal undernutrition during early pregnancy on growth, muscle cellularity, fiber type and carcass composition in lambs. Journal of Animal Science 64, 1419–1427.
PubMed |
open url image1

Oldham C , Ferguson M , Paganoni B , Thompson A , Kearney G , et al. (2005) The impact of the level of feed-on-offer available to Merino ewes during winter-spring on the wool production of their progeny as adults. In ‘Proceedings of the 20th international grasslands congress’. Dublin. (Eds FR O’Mara, RJ Wilkins, L ‘t Mannetje, DK Lovett, PAM Rogers, TM Boland) p. 138. (Wageningen Academic Publishers: Wageningen, The Netherlands)

Oliver MH, Hawkins P, Breier BH, Van Zijl PL, Sargison SA , et al. (2001) Maternal undernutrition during the periconceptual period increases plasma taurine levels and insulin response to glucose but not arginine in the late gestational fetal sheep. Endocrinology 142, 4576–4579.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Oliver MH, Breier BH, Gluckman PD, Harding JE (2002) Birth weight rather than maternal nutrition influences glucose tolerance, blood pressure, and IGF-I levels in sheep. Pediatric Research 52, 516–524.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Otten W, Kanitz E, Tuchscherer M, Nurnberg G (2001) Effects of prenatal restraint stress on hypothalamic–pituitary–adrenocortical and sympatho-adrenomedullary axis in neonatal pigs. Animal Science 73, 279–287. open url image1

Phillips ID, Simonetta G, Owens JA, Robinson JS, Clarke IJ , et al. (1996) Placental restriction alters the functional development of the pituitary–adrenal axis in the sheep fetus during late gestation. Pediatric Research 40, 861–866.
PubMed |
open url image1

Poore KR, Fowden AL (2002) The effect of birth weight on glucose tolerance in pigs at 3 and 12 months of age. Diabetologia 45, 1247–1254.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Poore KR, Fowden AL (2004) Insulin sensitivity in juvenile and adult Large White pigs of low and high birth weight. Diabetologia 47, 340–348.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Rhoads RP, Greenwood PL, Bell AW, Boisclair YR (2000) Nutritional regulation of the genes encoding the acid-labile subunit and other components of the circulating insulin-like growth factor system in the sheep. Journal of Animal Science 78, 2681–2689.
PubMed |
open url image1

Rich-Edwards J (2004) Epidemiology of the fetal origins of adult disease: cohort studies of birthweight and cardiovascular disease. In ‘Fetal nutrition and adult disease’. (Ed. SC Langley-Evans) pp. 87–104. (CABI Publishing: Wallingford, UK)

Rich-Edwards J, Stampfer MJ, Manson JE, Rosner B, Hankinson SE , et al. (1997) Birth weight and risk of cardiovascular disease in a cohort of women followed up since 1976. British Medical Journal 315, 396–400.
PubMed |
open url image1

Rich-Edwards JW, Colditz JA, Stampfer MJ, Willett WC, Gillman MW , et al. (1999) Birthweight and the risk for type 2 diabetes in adult women. Annals of Internal Medicine 130, 278–284.
PubMed |
open url image1

Schinckel PG, Short BF (1961) The influence of nutritional level during pre-natal and early post-natal life on adult fleece and body characteristics. Australian Journal of Agricultural Research 12, 176–202.
Crossref | GoogleScholarGoogle Scholar | open url image1

Symonds ME, Pearce S, Bispham J, Gardner DS, Stephenson T (2004) Timing of nutrient restriction and programming of fetal adipose development. The Proceedings of the Nutrition Society 63, 397–403.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Tuchscherer M, Kanitz E, Otten W, Tuchscherer A (2002) Effects of prenatal stress on cellular and humoral immune responses in neonatal pigs. Veterinary Immunology and Immunopathology 86, 195–203.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Warnes KE, Morris MJ, Symonds ME, Phillips ID, Clarke IJ, . (1998) Effects of increasing gestation, cortisol and maternal undernutrition on hypothalamic neuropeptide Y expression in the sheep fetus. Journal of Neuroendocrinology 10, 51–57.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Waterland RA, Jirtle RL (2004) Early nutrition, epigenetic changes at transposons and imprinted genes, and enhanced susceptibility to adult chronic diseases. Nutrition 20, 63–68.
Crossref | PubMed |
open url image1

Whorwood CB, Firth KM, Budge H, Symonds ME (2001) Maternal undernutrition during early to midgestation programs tissue-specific alterations in the expression of the glucocorticoid receptor, 11beta-hydroxysteroid dehydrogenase isoforms, and type 1 angiotensin II receptor in neonatal sheep. Endocrinology 142, 2854–2864.
Crossref | PubMed |
open url image1

Wintour EM, Moritz KM, Johnson K, Ricardo S, Samuel CS, Dodic M (2003) Reduced nephron number in adult sheep, hypertensive as a result of prenatal glucocorticoid treatment. Journal of Physiology 549, 929–935.
Crossref | PubMed |
open url image1