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RESEARCH ARTICLE

Effects of ewe size and nutrition during pregnancy on glucose metabolism, fat metabolism and adrenal function of postpubertal female twin offspring

D. S. van der Linden A B D E , P. R. Kenyon A B , H. T. Blair A B , N. Lopez-Villalobos A , C. M. C. Jenkinson A B , S. W. Peterson A B and D. D. S. Mackenzie B C
+ Author Affiliations
- Author Affiliations

A Institute of Veterinary, Animal and Biomedical Sciences, Sheep Research Group, Massey University, Palmerston North, New Zealand.

B National Research Centre for Growth and Development, Massey University, Palmerston North, New Zealand.

C Institute of Food, Nutrition and Human Health, Massey University, Palmerston North, New Zealand.

D Present address: Applied Biotechnology Group, AgResearch, Grasslands Research Centre, Palmerston North, New Zealand.

E Corresponding author. Email: danitsja.vanderlinden@agresearch.co.nz

Animal Production Science 50(9) 869-879 https://doi.org/10.1071/AN09131
Submitted: 5 October 2009  Accepted: 7 June 2010   Published: 29 September 2010

Abstract

Little is known about the long-term metabolic effects of maternal constraint on the offspring and whether a possible interaction of dam size and nutrition during gestation exists, affecting postnatal metabolic functions in the offspring. Four hundred and fifty heavy (H) (60.8 ± 0.18 kg) and 450 light (L) (42.5 ± 0.17 kg) Romney dams were allocated to ad libitum (A) or maintenance (M) nutritional regimens under New Zealand pastoral grazing conditions, from Day 21 to 140 after insemination. One week before lambing, all dams and offspring were managed as one group and provided with ad libitum feeding. At 16 months of age, female twin-born offspring (n = 12 per size by nutrition group) were catheterised and given intravenous insulin (0.15 IU/kg) (ITT), glucose (0.17 g/kg) (GTT) and epinephrine (1 μg/kg) (ETT) challenges to assess their glucose and fat metabolism and adrenal function. No effects of dam size or interactions between dam size and dam nutrition were found on glucose or fat metabolism or adrenal function. In response to the ETT, M-dam offspring showed greater (P < 0.05) peak glucose concentrations, increased (P < 0.05) glucose area under the curve and tended (P < 0.10) to have increased maximum change in glucose and non-esterified free fatty acid concentrations compared with A-ewes. No effects of dam nutrition were found on glucose tolerance, insulin resistance or adrenal function in response to GTT and ITT. In conclusion, dam size had no effect on glucose metabolism, adrenal function or fat metabolism in 16-month-old female twin offspring. Dam nutrition during pregnancy from Day 21 to 140 had no major effect on glucose metabolism, adrenal function or lipolysis; however, it did potentially affect gluconeogenesis and/or glycogenolysis, as increased glucose concentrations in ewes born to M-fed dams were observed in response to ETT. These results indicate that M-ewes could have an advantage over A-ewes in physiological stressful situations in life (e.g. pregnancy, lactation) as their liver may be able to supply more glucose to support their growing conceptus and milk production to increase the chances of survival of their offspring.


Acknowledgements

The authors would like to thank Florence Delassus, who assisted with all the animal work and data collection, Dr Mark Oliver at Auckland University for his helpful advice, the team at IVABS for their help with blood collection and Eric Thorstensen at Auckland University for the blood analyses. The authors are grateful to Massey University, Meat and Wool New Zealand and the National Research Centre for Growth and Development for providing funding assistance for this project. The senior author is funded by an AGMARDT doctoral scholarship.


References


Allen WR, Wilsher S, Turnbull C, Stewart F, Ousey J, Rossdale PD, Fowden AL (2002) Influence of maternal size on placental, fetal and postnatal growth in the horse. I. Development in utero. Reproduction 123, 445–453.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Baschat AA (2006) The fetal circulation and essential organs – a new twist to an old tale. Ultrasound in Obstetrics & Gynecology 27, 349–354.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Basset JM (1970) Metabolic effects of catecholamines in sheep. Australian Journal of Agricultural Science 23, 903–914. open url image1

Bloomfield FH, Oliver MH, Giannoulias CD, Gluckman PD, Harding JE, Challis JRG (2003) Brief undernutrition in late-gestation sheep programs the hypothalamic-pituitary-adrenal axis in adult offspring. Endocrinology 144, 2933–2940.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Burdge GC, Phillips ES, Dunn RL, Jackson AA, Lillycrop KA (2004) Effect of reduced maternal protein consumption during pregnancy in the rat on plasma lipid concentrations and expression of peroxisomal proliferator-activated receptors in the liver and adipose tissue of the offspring. Nutrition Research 24, 639–646.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Carter ML, McCutcheon SN, Purchas RW (1989) Plasma metabolite and hormone concentrations as predictors of genetic merit of lean meat production in sheep: effects of metabolic challenges and fasting. New Zealand Journal of Agricultural Research 32, 343–353. open url image1

Chapa AM, Fernandez JM, Thompson DL (1997) Changes in plasma somatotropin, prolactin, glucose, and nonesterified fatty acid concentrations in goats administered an epinephrine challenge. Small Ruminant Research 23, 125–133.
Crossref | GoogleScholarGoogle Scholar | open url image1

de Rooij SR, Painter RC, Roseboom TJ, Osmond C, Phillips DIW, Barker DJP, Tanck MW, Michels RPJ, Bossuyt PMM, Bleker OP (2006) Glucose tolerance at age 58 and the decline of glucose tolerance in comparison with age 50 in people prenatally exposed to the Dutch famine. Diabetologia 49, 637–643.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Desai M, Byrne CD, Meeran K, Martenz ND, Bloom SR, Hales CN (1997) Regulation of hepatic enzymes and insulin levels in offspring of rat dams fed a reduced-protein diet. American Journal of Physiology. Gastrointestinal and Liver Physiology 273, G899–G904.
CAS |
open url image1

Dickinson AG, Hancock JL, Hovell GJR, Taylor SCS, Wiener G (1962) The size of lambs at birth – a study involving egg transfer. Animal Production 4, 64–79.
Crossref |
open url image1

Durrington PN, Newton RS, Weinstein DB, Steinberg D (1982) Effect of insulin and glucose on very low density lipoprotein triglyceride secretion by cultured rat hepatocytes. The Journal of Clinical Investigation 70, 63–73.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Fernandez-Twinn DS, Wayman A, Ekizoglou S, Martin MS, Hales CN, Ozanne SE (2005) Maternal protein restriction leads to hyperinsulinemia and reduced insulin-signaling protein expression in 21-mo-old female rat offspring. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 288, R368–R373.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Ferrell CL (1991a) Maternal and foetal influences on uterine and conceptus development in the cow: I. Growth of the tissues of the gravid uterus. Journal of Animal Science 69, 1945–1953.
CAS | PubMed |
open url image1

Ferrell CL (1991b) Maternal and foetal influences on uterine and conceptus development in the cow: II. Blood flow and nutrient flux. Journal of Animal Science 69, 1954–1965.
CAS | PubMed |
open url image1

Firth EC, Rogers CW, Vickers M, Kenyon PR, Jenkinson CMC, Blair HT, Johnson PL, Mackenzie DDS, Peterson SW, Morris ST (2008) The bone-muscle ratio of fetal lambs is affected more by maternal nutrition during pregnancy than by maternal size. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 294, R1890–R1894.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Ford SP, Hess BW, Schwope MM, Nijland MJ, Gilbert JS, Vonnahme KA, Means WJ, Han H, Nathanielsz PW (2007) Maternal undernutrition during early to mid-gestation in the ewe results in altered growth, adiposity, and glucose tolerance in male offspring. Journal of Animal Science 85, 1285–1294.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Gardner DS, Tingey K, Van Bon BWM, Ozanne SE, Wilson V, Dandrea J, Keisler DH, Stephenson T, Symonds ME (2005) Programming of glucose-insulin metabolism in adult sheep after maternal undernutrition. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 289, R947–R954.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Gardner DS, Van Bon BWM, Dandrea J, Goddard PJ, May SF, Wilson V, Stephenson T, Symonds ME (2006) Effect of periconceptional undernutrition and gender on hypothalamic-pituitary-adrenal axis function in young adult sheep. The Journal of Endocrinology 190, 203–212.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Gardner DS, Bell RC, Symonds ME (2007) Fetal mechanisms that lead to later hypertension. Current Drug Targets 8, 894–905.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Gatford KL, Wintour EM, De Blasio MJ, Owens JA, Dodic M (2000) Differential timing for programming of glucose homeostasis, sensitivity to insulin and blood pressure by in utero exposure to dexamethasone in sheep. Clinical Science 98, 553–560.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Geenty KG , Rattray PV (1987) The energy requirements of grazing sheep and cattle. In ‘Livestock feeding on pasture’. (Ed. AM Nicol) pp. 39–53. (Bascands Ltd: Hamilton)

Gluckman PD, Hanson MA, Spencer GS (2005) Predictive adaptive responses and human evolution. Trends in Ecology & Evolution 20, 527–533.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gootwine E, Bor A, Brawtal R, Zenou A (1993) Inheritance of birth-weight and growth traits in crosses between the Booroola Merino and Assaf sheep breeds. Livestock Production Science 33, 119–126.
Crossref | GoogleScholarGoogle Scholar | 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.
CAS | PubMed |
open url image1

Hales CN, Barker DJP (2001) The thrifty phenotype hypothesis. British Medical Bulletin 60, 5–20.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Haugen G, Hanson M, Kiserud T, Crozier S, Inskip H, Godfrey KM (2005) Fetal liver-sparing cardiovascular adaptations linked to mother’s slimness and diet. Circulation Research 96, 12–14.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Hawkins P, Steyn C, McGarrigle HHG, Calder NA, Saito T, Stratford LL, Noakes DE, Hanson MA (2000) Cardiovascular and hypothalamic-pituitary-adrenal 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 | CAS | open url image1

Husted SM, Nielsen MO, Blache D, Ingvartsen KL (2008) Glucose homeostasis and metabolic adaption in the pregnant and lactating sheep are affected by the level of nutrition previously provided during her late fetal life. Domestic Animal Endocrinology 34, 419–431.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Jocken JWE, Blaak EE (2008) Catecholamine-induced lipolysis in adipose tissue and skeletal muscle in obesity. Physiology & Behavior 94, 219–230.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Kenyon PR (2008) A review of in-utero environmental effects on sheep production. Proceedings of the New Zealand Society of Animal Production 68, 142–155. open url image1

Kenyon PR, Blair HT, Jenkinson CMC, Morris ST, Mackenzie DDS, Peterson SW, Firth EC, Johnston PL (2009) The effect of ewe size and nutrition regimen beginning in early pregnancy on ewe and lamb performance to weaning. New Zealand Journal of Agricultural Research 52, 203–212.
Crossref |
open url image1

McCurdy CE, Friedman JE (2006) Early foetal programming of hepatic gluconeogenesis: glucocorticoids strike back. Diabetologia 49, 1138–1141.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

McDowell GH (1983) Hormonal control of glucose homeostasis in ruminants. The Proceedings of the Nutrition Society 42, 149–167.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Mellor DJ (1983) Nutritional and placental determinants of fetal growth-rate in sheep and consequences for the newborn lamb. The British Veterinary Journal 139, 307–324.
CAS | PubMed |
open url image1

Newsome CA, Shiell AW, Fall CHD, Phillips DIW, Shier R, Law CM (2003) Is birth weight related to later glucose and insulin metabolism? A systematic review. Diabetic Medicine 20, 339–348.
Crossref | GoogleScholarGoogle Scholar | CAS | 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.
CAS | PubMed |
open url image1

Ravelli ACJ, van der Meulen JHP, Michels RPJ, Osmond C, Barker DJP, Hales CN, Bleker OP (1998) Glucose tolerance in adults after prenatal exposure to famine. Lancet 351, 173–177.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Ravelli ACJ, van der Meulen JHP, Osmond C, Barker DJP, Bleker OP (1999) Obesity at the age of 50 years in men and women exposed to famine prenatally. The American Journal of Clinical Nutrition 70, 811–816.
CAS | PubMed |
open url image1

Robinson JJ, Sinclair KD, McEvoy TG (1999) Nutritional effects on foetal growth. Animal Science 68, 315–331. open url image1

Roseboom TJ, van der Meulen JHP, Osmond C, Barker DJP, Ravelli ACJ, Bleker OP (2000) Plasma lipid profiles in adults after prenatal exposure to the Dutch famine. The American Journal of Clinical Nutrition 72, 1101–1106.
CAS | PubMed |
open url image1

Rumball CWH, Harding JE, Oliver MH, Bloomfield FH (2008a) Effects of twin pregnancy and periconceptional undernutrition on maternal metabolism, fetal growth and glucose-insulin axis function in ovine pregnancy. Journal of Physiology-London 586, 1399–1411.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Rumball CWH, Oliver MH, Thorstensen EB, Jaquiery AL, Husted SM, Harding JE, Bloomfield FH (2008b) Effects of twinning and periconceptional undernutrition on late-gestation hypothalamic-pituitary-adrenal axis function in ovine pregnancy. Endocrinology 149, 1163–1172.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Sloboda DM, Moss TJM, Li SF, Doherty DA, Nitsos I, Challis JRG, Newnham JP (2005) Hepatic glucose regulation and metabolism in adult sheep: effects of prenatal betamethasone. American Journal of Physiology. Endocrinology and Metabolism 289, E721–E728.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Symonds ME (2007) Integration of physiological and molecular mechanisms of the developmental origins of adult disease: new concepts and insights. The Proceedings of the Nutrition Society 66, 442–450.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

van der Linden DS, Kenyon PR, Jenkinson CMC, Peterson SW, Lopez-Villalobos N, Blair HT (2007) The effects of ewe size and nutrition during pregnancy on growth and onset of puberty in female progeny. Proceedings of the New Zealand Society of Animal Production 67, 126–129. open url image1

Vernon RG (1981) Lipid metabolism in the adipose tissue of ruminant animals. In ‘Lipid metabolism in ruminant animals’. (Ed. WW Christie) pp. 279–362. (Pergamon Press: Oxford)

Walton A, Hammond J (1938) The maternal effects on growth and conformation in Shire horse-Shetland pony crosses. Proceedings of the Royal Society of London. Series B. Biological Sciences 125, 311–335.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wilson ME, Biensen NJ, Youngs CR, Ford SP (1998) Development of Meishan and Yorkshire littermate conceptuses in either a Meishan or Yorkshire uterine environment to day 90 of gestation and to term. Biology of Reproduction 58, 905–910.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Wu G, Bazer FW, Wallace JM, Spencer TE (2006) Board-invited review: intrauterine growth retardation: implications for the animal sciences. Journal of Animal Science 84, 2316–2337.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1