Hostname: page-component-848d4c4894-xm8r8 Total loading time: 0 Render date: 2024-06-19T01:36:21.211Z Has data issue: false hasContentIssue false
  • English
  • Français

Relationships between early postnatal growth and metabolic function of 16-month-old female offspring born to ewes exposed to different environments during pregnancy

Published online by Cambridge University Press:  22 December 2009

D. S. van der Linden ,
P. R. Kenyon ,
H. T. Blair ,
N. Lopez-Villalobos ,
C. M. C. Jenkinson ,
S. W. Peterson  and
D. D. S. Mackenzie
D. S. van der Linden*
Affiliation:
Sheep Research Group, Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Palmerston North, New Zealand National Research Centre for Growth and Development, Massey University, Palmerston North, New Zealand
P. R. Kenyon
Affiliation:
Sheep Research Group, Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Palmerston North, New Zealand National Research Centre for Growth and Development, Massey University, Palmerston North, New Zealand
H. T. Blair*
Affiliation:
Sheep Research Group, Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Palmerston North, New Zealand National Research Centre for Growth and Development, Massey University, Palmerston North, New Zealand
N. Lopez-Villalobos
Affiliation:
Sheep Research Group, Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Palmerston North, New Zealand
C. M. C. Jenkinson
Affiliation:
Sheep Research Group, Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Palmerston North, New Zealand National Research Centre for Growth and Development, Massey University, Palmerston North, New Zealand
S. W. Peterson
Affiliation:
Sheep Research Group, Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Palmerston North, New Zealand National Research Centre for Growth and Development, Massey University, Palmerston North, New Zealand
D. D. S. Mackenzie
Affiliation:
Sheep Research Group, Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Palmerston North, New Zealand Institute of Food, Nutrition and Human Health, Massey University, Palmerston North, New Zealand
*
Address for correspondence: D. S. van der Linden or H. T. Blair, Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Tennant Drive, Palmerston North, New Zealand 4442. (Email D.vanderLinden@massey.ac.nz, H.Blair@massey.ac.nz)
Address for correspondence: D. S. van der Linden or H. T. Blair, Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Tennant Drive, Palmerston North, New Zealand 4442. (Email D.vanderLinden@massey.ac.nz, H.Blair@massey.ac.nz)
Get access Rights & Permissions [Opens in a new window]

Abstract

It was hypothesized that exposure of the fetus to adverse conditions in utero due to either maternal constraint or nutrition may result in developmental adaptations altering metabolism and postnatal growth of the offspring. Heavy (H) and light (L) Romney dams (G0) were allocated to ad libitum (A) or maintenance (M) nutritional regimens, from day 21–day 140 of pregnancy. Female twin-born offspring (G1) born to the dams in the four treatment groups will be referred to as HA-ewes, LA-ewes, HM-ewes and LM-ewes. At 16 months of age, offspring were catheterized and given intravenous insulin tolerance test (ITT), glucose tolerance test (GTT) and epinephrine tolerance test challenges to assess their glucose and fat metabolism in relation to their birth weight and postnatal growth. In HA-ewes, the regression coefficients of growth rates prior to puberty on insulin and glucose curves in response to GTT (InsAUCGTT) and ITT (GluAUCITT), respectively, were different from 0 (P < 0.05) and were different from the regression coefficients of HM-ewes. This may indicate that HA-ewes may have showed puberty-related insulin resistance at 16 months of age with increasing growth rates prior to puberty compared to HM- or LM-ewes. In HM-ewes, the regression coefficients of growth rates after puberty on InsAUCGTT and GluAUCITT were different from 0 (P < 0.05) and were different from those of HA-ewes. These results may indicate that offspring born to heavy dams fed maintenance during pregnancy and with greater postnatal growth rates after puberty could develop glucose intolerance and insulin resistance in later life.

Keywords

glucose intolerance, growth, maternal nutrition, maternal progeny, sheep, size
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 1 , Issue 1 , February 2010 , pp. 50 - 59
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1.Wu, G, Bazer, FW, Wallace, JM, Spencer, TE. Board-invited review: intrauterine growth retardation: implications for the animal sciences. J Anim Sci. 2006; 84, 2316–2337.CrossRefGoogle ScholarPubMed
2.Oliver, MH, Breier, BH, Gluckman, PD, Harding, JE. Birth weight rather than maternal nutrition influences glucose tolerance, blood pressure, and IGF-I levels in sheep. Pediatr Res. 2002; 52, 516–524.CrossRefGoogle ScholarPubMed
3.Gardner, DS, Tingey, K, Van Bon, BWM, et al. Programming of glucose-insulin metabolism in adult sheep after maternal undernutrition. Am J Physiol Regul Integr Comp Physiol. 2005; 289, R947–R954.CrossRefGoogle ScholarPubMed
4.Ford, SP, Hess, BW, Schwope, MM, et al. Maternal undernutrition during early to mid-gestation in the ewe results in altered growth, adiposity, and glucose tolerance in male offspring. J Anim Sci. 2007; 85, 1285–1294.CrossRefGoogle ScholarPubMed
5.Hawkins, P, Steyn, C, McGarrigle, HHG, et al. Cardiovascular and hypothalamic-pituitary-adrenal axis development in late gestation fetal sheep and young lambs following modest maternal nutrient restriction in early gestation. Reprod Fert Develop. 2000; 12, 443–456.CrossRefGoogle Scholar
6.Bloomfield, FH, Oliver, MH, Giannoulias, CD, et al. Brief undernutrition in late-gestation sheep programs the hypothalamic-pituitary-adrenal axis in adult offspring. Endocrinology. 2003; 144, 2933–2940.CrossRefGoogle ScholarPubMed
7.Gardner, DS, Van Bon, BWM, Dandrea, J, et al. Effect of periconceptional undernutrition and gender on hypothalamic-pituitary-adrenal axis function in young adult sheep. J Endocrinol. 2006; 190, 203–212.CrossRefGoogle ScholarPubMed
8.Greenwood, PL, Hunt, AS, Hermanson, JW, Bell, AW. Effects of birth weight and postnatal nutrition on neonatal sheep: I. Body growth and composition, and some aspects of energetic efficiency. J Anim Sci. 1998; 76, 2354–2367.CrossRefGoogle ScholarPubMed
9.Mellor, DJ. Nutritional and placental determinants of fetal growth-rate in sheep and consequences for the newborn lamb. Brit Vet J. 1983; 139, 307–324.CrossRefGoogle ScholarPubMed
10.Dickinson, AG, Hancock, JL, Hovell, GJR, Taylor, SCS, Wiener, G. The size of lambs at birth – A study involving egg transfer. Anim Prod. 1962; 4, 64–79.Google Scholar
11.Gootwine, E, Bor, A, Brawtal, R, Zenou, A. Inheritance of birth-weight and growth traits in crosses between the Booroola Merino and Assaf sheep breeds. Livest. Prod. Sci.. 1993; 33, 119–126.CrossRefGoogle Scholar
12.Walton, A, Hammond, J. The maternal effects on growth and conformation in Shire horse-Shetland pony crosses. Proc Roy Soc Lond B Biol Sci. 1938; 125, 311–335.Google Scholar
13.Allen, WR, Wilsher, S, Turnbull, C, et al. Influence of maternal size on placental, fetal and postnatal growth in the horse. I. Development in utero. Reproduction. 2002; 123, 445–453.CrossRefGoogle ScholarPubMed
14.Wilson, ME, Biensen, NJ, Youngs, CR, Ford, SP. Development of Meishan and Yorkshire littermate conceptuses in either a Meishan or Yorkshire uterine environment to day 90 of gestation and to term. Biol Reprod. 1998; 58, 905–910.CrossRefGoogle ScholarPubMed
15.Desai, M, Hales, CN. Role of fetal and infant growth in programming metabolism in later life. Biol Rev Camb Philos Soc. 1997; 72, 329–348.CrossRefGoogle ScholarPubMed
16.Cottrell, EC, Ozanne, SE. Early life programming of obesity and metabolic disease. Physiol Behav. 2008; 94, 17–28.CrossRefGoogle ScholarPubMed
17.Bloomfield, FH, Oliver, MH, Harding, JE. Effects of twinning, birth size, and postnatal growth on glucose tolerance and hypothalamic-pituitary-adrenal function in postpubertal sheep. Am J Physiol Endocrinol Metab. 2007; 292, E231–E237.CrossRefGoogle ScholarPubMed
18.Eriksson, JG, Forsen, T, Tuomilehto, J, et al. Effects of size at birth and childhood growth on the insulin resistance syndrome in elderly individuals. Diabetologia. 2002; 45, 342–348.CrossRefGoogle ScholarPubMed
19.Ozanne, SE, Hales, CN. Poor fetal growth followed by rapid postnatal catch-up growth leads to premature death. Mech Ageing Dev. 2005; 126, 852–854.CrossRefGoogle ScholarPubMed
20.Firth, EC, Rogers, CW, Vickers, M, et al. The bone-muscle ratio of fetal lambs is affected more by maternal nutrition during pregnancy than by maternal size. Am J Physiol Regul Integr Comp Physiol. 2008; 294, R1890–R1894.CrossRefGoogle ScholarPubMed
21.Kenyon, PR, Blair, HT, Jenkinson, CMC, et al. The effect of ewe size and nutrition regimen beginning in early pregnancy on ewe and lamb performance to weaning. N Z J Agric Res. 2009; 52, 203–212.CrossRefGoogle Scholar
22.van der Linden, DS, Kenyon, PR, Jenkinson, CMC, et al. The effects of ewe size and nutrition during pregnancy on growth and onset of puberty in female progeny. Proc N Z Soc Anim Prod. 2007; 67, 126–129.Google Scholar
23.Geenty, KG, Rattray, PV. The energy requirements of grazing sheep and cattle. In Livestock Feeding on Pasture (ed. Nicol AM), 1987; pp. 39–53. Bascands Ltd: Hamilton, New Zealand.Google Scholar
24.Rumball, CWH, Harding, JE, Oliver, MH, Bloomfield, FH. Effects of twin pregnancy and periconceptional undernutrition on maternal metabolism, fetal growth and glucose-insulin axis function in ovine pregnancy. J Physiol Lond. 2008; 586, 1399–1411.CrossRefGoogle ScholarPubMed
25.Rumball, CWH, Oliver, MH, Thorstensen, EB, et al. Effects of twinning and periconceptional undernutrition on late-gestation hypothalamic-pituitary-adrenal axis function in ovine pregnancy. Endocrinology. 2008; 149, 1163–1172.CrossRefGoogle ScholarPubMed
26.SAS. Statistical Analysis System. 9.1. 2006. SAS Institute Inc., Cary, NC, USA.Google Scholar
27.Narum, SR. Beyond Bonferroni: Less conservative analyses for conservation genetics. Conser Gen. 2006; 7, 783–787.CrossRefGoogle Scholar
28.Eriksson, JG, Osmond, C, Kajantie, E, Forsen, TJ, Barker, DJP. Patterns of growth among children who later develop type 2 diabetes or its risk factors. Diabetologia. 2006; 49, 2853–2858.CrossRefGoogle ScholarPubMed
29.Amiel, SA, Caprio, S, Sherwin, RS, et al. Insulin resistance of puberty – A defect restricted to peripheral glucose-metabolism. J Clin Physiol Endocrin Metab. 1991; 72, 277–282.CrossRefGoogle ScholarPubMed
30.Moran, A, Jacobs, DR, Steinberger, J, et al. Insulin resistance during puberty – Results from clamp studies in 357 children. Diabetes. 1999; 48, 2039–2044.CrossRefGoogle ScholarPubMed
31.Gower, BA, Caprio, S. Puberty, insulin resistance, and type 2 diabetes. In Handbook of Pediatric Obesity: Etiology, Pathophysiology, and Prevention (ed. Goran MI), 2006; pp. 175–196. CRC Press-Taylor & Francis Group: Boca Raton, FL, USA.Google Scholar
32.Moran, A, Jacobs, DR, Steinberger, J, et al. Association between the insulin resistance of puberty and the insulin-like growth factor-I/growth hormone axis. J Clin Endocrino Metab. 2002; 87, 4817–4820.CrossRefGoogle ScholarPubMed
33.Keller, U, Miles, JM. Growth-hormone and lipids. In 2nd Symp on hGH (human Growth Hormone). Horm Res. 1991; 36(Suppl. 1), 36–40.Google Scholar
34.Symonds, ME. Integration of physiological and molecular mechanisms of the developmental origins of adult disease: new concepts and insights. Proc Nutr Soc. 2007; 66, 442–450.CrossRefGoogle ScholarPubMed
35.Davies, MJ, Rayman, G, Grenfell, A, et al. Loss of the 1st phase insulin-response to intravenous glucose in subjects with persistent impaired glucose-tolerance. Diabet Med. 1994; 11, 432–436.CrossRefGoogle Scholar
36.Fernandez-Twinn, DS, Wayman, A, Ekizoglou, S, et al. Maternal protein restriction leads to hyperinsulinemia and reduced insulin-signaling protein expression in 21-mo-old female rat offspring. Am J Physiol Regul Integr Comp Physiol. 2005; 288, R368–R373.CrossRefGoogle ScholarPubMed
37.Ozanne, SE, Wang, CL, Dorling, MW, Petry, CJ. Dissection of the metabolic actions of insulin in adipocytes from early growth-retarded male rats. J Endocrinol. 1999; 162, 313–319.CrossRefGoogle ScholarPubMed
38.Prentice, AM. Early influences on human energy regulation: thrifty genotypes and thrifty phenotypes. Physiol Behav. 2005; 86, 640–645.CrossRefGoogle ScholarPubMed
39.Vernon, RG. Lipid metabolism in the adipose tissue of ruminant animals. In Lipid metabolism in ruminant animals (ed. Christie WW), 1981; pp. 279–362. Pergamon Press Ltd: Oxford, New York.CrossRefGoogle Scholar