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The effect of overnourishing singleton-bearing adult ewes on nutrient partitioning to the gravid uterus

Published online by Cambridge University Press:  08 March 2007

Jacqueline M. Wallace ,
John S. Milne  and
Raymond P. Aitken
Jacqueline M. Wallace*
Affiliation:
Rowett Research Institute, Bucksburn, Aberdeen AB21 9SB, UK
John S. Milne
Affiliation:
Rowett Research Institute, Bucksburn, Aberdeen AB21 9SB, UK
Raymond P. Aitken
Affiliation:
Rowett Research Institute, Bucksburn, Aberdeen AB21 9SB, UK
*
*Corresponding author: Dr Jacqueline M. Wallace, fax +44 1224 716622, email Jacqueline.Wallace@rri.sari.ac.uk
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Abstract

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Overnourishing the singleton-bearing adolescent sheep throughout pregnancy promotes maternal tissue synthesis at the expense of the nutrient requirements of the gravid uterus. Consequently, the growth of the placenta is impaired and results in the premature delivery of low-birth-weight lambs relative to moderately fed adolescents of equivalent age. To establish if this phenomenon is unique to the growing animal, singleton pregnancies to a single sire were established by embryo transfer into primiparous adult ewes who had attained the normal mature body size for their genotype. Thereafter ewes were offered a maintenance or a high level of a complete diet throughout gestation. High maternal intakes resulted in elevated maternal insulin, no significant change in growth hormone or glucose, and attenuated progesterone and NEFA concentrations. Live weight gain during the first 93 d of gestation was 48 and 244 g/d, and adiposity score at term was 2·4 and 3·7 in the maintenance and high groups, respectively (P<0·001). In spite of achieving levels of adiposity similar to overnourished adolescents, placental (477 (sem 30) v. 518 (sem 41) g) and fetal (5190 (sem 320) v. 5420 (sem 250) g) weights were equivalent in maintenance and high groups. Gestation length was shorter (P<0·01) and colostrum yield at parturition lower (P<0·05) in high v. maintenance dams. Thus, adult sheep appear to be relatively insensitive to the oversupply of nutrients during pregnancy and have the ability to meet the nutrient requirements for normal conceptus growth in spite of their increased adiposity.

Keywords

PregnancyNutrient partitioningFetusPlacentaBody composition
Type
Research Article
Information
British Journal of Nutrition , Volume 94 , Issue 4 , October 2005 , pp. 533 - 539
Copyright
Copyright © The Nutrition Society 2005

References

Barcroft, J (1946) Researches on Prenatal Life. Oxford: Blackwell Scientific Publications.Google Scholar
Bell, AW & Bauman, DE (1997) Adaptations of glucose metabolism during pregnancy and lactation. J Mammary Gland Biol Neoplasia 2, 265–278.Google Scholar
Castro, LC & Avina, RL (2002) Maternal obesity and pregnancy outcomes. Curr Opin Obstet Gynecol 14, 601–606.Google Scholar
Cnattingius, S, Bergstrom, R, Lipworth, L & Kramer, MS (1998) Prepregnancy weight and the risk of adverse pregnancy outcomes. N Engl J Med 338, 147–152.Google Scholar
Cumming, IA, Blockey, MADWinfield, CG, Parr, RA & Williams, AH (1975) A study of the relationships of breed, time of mating, level of nutrition, live weight, body condition, and face cover to embryo survival in ewes. J Agric Sci 84, 559–565.Google Scholar
Fleming, TP, Kwong, WY, Porter, R, Ursell, E, Fesenko, I, Wilkins, A, Miller, DJ, Watkins, AJ & Eckert, JJ (2004) The embryo and its future. Biol Reprod 71, 1046–1054.Google Scholar
Greenwood, PL & Bell, AW (2002) Consequences of intra-uterine growth retardation for postnatal growth, metabolism and pathophysiology. Reprod Suppl 61, 195–206.Google Scholar
Guesnet, M, Massoud, MJ & Demarne, Y (1991) Regulation of adipose tissue metabolism during pregnancy and lactation in the ewe: the role of insulin. J Anim Sci 69, 2057–2065.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. Paediatr Res 44, 546–551.Google Scholar
Hilson, JA, Rasmussen, KM & Kjolhede, CL (2004) High prepregnant body mass index is associated with poor lactation outcomes among white, rural women independent of psychosocial and demographic correlates. J Hum Lact 20, 18–29.Google Scholar
Kelly, RW (1992) Nutrition and placental development. Proc Nutr Soc Aust 17, 203–211.Google Scholar
Kirchengast, S & Hartmann, B (2003) Impact of maternal age and maternal somatic characteristics on newborn size. Am J Hum Biol 15, 220–228.Google Scholar
Kramer, MS (2002) Balanced protein/energy supplementation in pregnancy. Cochrane Database Syst Rev 2, CD000032.Google Scholar
MacRae, JC, Bruce, LA, Hovell, FD, Hart, IC, Inkster, J, Walker, A & Atkinson, T (1991) Influence of protein nutrition on the response of growing lambs to exogenous bovine growth hormone. J Endocrinol 130, 53–61.Google Scholar
Mathews, F, Yudkin, P & Neil, A (1999) Influence of maternal nutrition on outcome of pregnancy: prospective cohort study. Br Med J 319, 339–343.Google Scholar
Matsubara, C, Nishikawa, Y, Yoshida, Y & Takamura, K (1983) A spectrophotometric method for the determination of free fatty acids in serum using acyl-coenzyme A synthetase and acyl coenzyme A oxidase. Anal Biochem 130, 128–133.Google Scholar
Mellor, DJ (1983) Nutritional and placental determinants of foetal growth rate in sheep and consequences for the newborn lamb. Br Vet J 139, 307–324.Google Scholar
Muhlhausler, BS, Roberts, CT, McFarlane, JR, Kauter, KG & McMillen, IC (2002) Fetal leptin is a signal of fat mass independent of maternal nutrition in ewes fed at or above maintenance energy requirements. Biol Reprod 67, 493–499.Google Scholar
Oddy, VH & Holst, PJ (1991) Maternal–foetal adaptation to mid pregnancy feed restriction in single-bearing ewes. Aust J Agric Res 42, 969–978.Google Scholar
Olausson, PO, Cnattingius, S & Haglund, B (1999) Teenage pregnancies and risk of late foetal death and infant mortality. Br J Obstet Gynaecol 106, 116–121.Google Scholar
Parr, RA (1992) Nutrition–progesterone interactions during early pregnancy in sheep. Reprod Fertil Dev 4, 297–300.Google Scholar
Parr, RA, Williams, AH, Cambell, IP, Witcome, GF & Roberts, AM (1986) Low nutrition of ewes in early pregnancy and the residual effect on the offspring. J Agric Sci (Camb) 106, 81–87.Google Scholar
Parr, RA, Davis, IF, Fairclough, RJ & Miles, MA (1987) Overfeeding during early pregnancy reduces peripheral progesterone concentration and pregnancy rate in sheep. J Reprod Fertil 80, 317–320.Google Scholar
Peterson, JI & Young, DS (1968) Evaluation of hexokinase/glucose-6-phosphate dehydrogenase method of determination of glucose in urine. Anal Biochem 23, 301–316.Google Scholar
Rasmussen, KM, Hilson, JA & Kjolhede, CL (2002) Obesity is a risk factor for failure to initiate and sustain lactation. Adv Exp Med Biol 503, 217–222.Google Scholar
Robinson, JJ (1983) Nutrition of the pregnant ewe. Sheep Production, pp.111– 131 [Haresign, W, editor]. London: Butterworths.Google Scholar
Robinson, JJ, Sinclair, KD & McEvoy, TG (1999) Nutritional effects on foetal growth. Anim Sci 68, 315–331.Google Scholar
Ronayne, E & Hynes, N (1990) Measurement of plasma progesterone concentrations by extraction and non-extraction radioimmunoassays. Irish J Agric Res 29, 109–115.Google Scholar
Russel, AJF, Doney, JM & Reid, RL (1967) The use of biochemical parameters in controlling nutritional state in pregnant ewes, and the effects of undernourishment during pregnancy on lamb birth-weight. J Agric Sci (Camb) 68, 351–358.Google Scholar
Russel, AJF, Doney, JM & Gunn, RG (1969) Subjective assessment of body fat in live sheep. J Agric Sci (Camb) 72, 451–454.Google Scholar
Schieve, LA, Cogswell, ME, Scanlon, KS, Perry, G, Ferre, C, Blackmore-Prince, C, Yu, SM & Rosenberg, D (2000) Prepregnancy body mass index and pregnancy weight gain: associations with preterm delivery. Obstet Gynecol 96, 194–200.Google Scholar
Scottish Needs Assessment Programme (1994) Teenage Pregnancy in Scotland – Report. Glasgow: Scottish Forum for Public Health Medicine.Google Scholar
Sloan, NL, Lederman, SA, Leighton, J, Himes, JH & Rush, D (2001) The effect of prenatal dietary protein intake on birth weight. Nutr Res 21, 129–139.Google Scholar
Stephansson, O, Dickman, PW, Johansson, A & Cnattingius, S (2001) Maternal weight, prepregnancy weight gain, and the risk of antepartum stillbirth. Am J Obstet Gynecol 184, 463–469.Google Scholar
Steyn, C, Hawkins, P, Saito, T, Noakes, DE, Kingdom, JCP & Hanson, MA (2001) Undernutrition during the first half of gestation increases the predominance of foetal tissue in late gestation ovine placentomes. Eur J Obstet Gynecol Reprod Biol 98, 165–170.Google Scholar
Symonds, ME, Budge, H, Stephenson, T & McMillen, IC (2001) Fetal endocrinology and development – manipulation and adaptation to long-term nutritional and environmental challenges. Reproduction 121, 853–862.Google Scholar
Thomas, L, Wallace, JM, Aitken, RP, Mercer, JG, Trayhurn, P & Hoggard, N (2001) Circulating leptin during ovine pregnancy in relation to maternal nutrition, body composition and pregnancy outcome. J Endocrinol 169, 465–476.Google Scholar
Vernon, RG, Clegg, RA & Flint, DJ (1981) Metabolism of sheep adipose tissue during pregnancy and lactation. Biochem J 200, 307–314.Google Scholar
Vonnahme, KA, Hess, BW & Hansen, TR (2003) Maternal undernutrition from early- to mid-gestation leads to growth retardation, cardiac ventricular hypertrophy, and increased liver weight in fetal sheep. Biol Reprod 69, 133–140.Google Scholar
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. Reprod Fertil Dev 6, 253–259.Google Scholar
Wallace, JM, Aitken, RP & Cheyne, MA (1996) Nutrient partitioning and fetal growth in rapidly growing adolescent ewes. J Reprod Fertil 107, 183–190.Google Scholar
Wallace, JM, Da Silva, P, Aitken, RP & Cheyne, MA (1997 a) Maternal endocrine status in relation to pregnancy outcome in rapidly growing adolescent sheep. J Endocrinol 155, 359–368.Google Scholar
Wallace, JM, Aitken, RP, Cheyne, MA & Humblot, P (1997b) Pregnancy specific protein B and progesterone concentrations in relation to nutritional regimen, placental mass and pregnancy outcome in growing adolescent ewes carrying singleton fetuses. J Reprod Fertil 109, 53–58.Google Scholar
Wallace, JM, Bourke, DA & Aitken, RP (1999 a) Nutrition and fetal growth: paradoxical effects in the overnourished adolescent sheep. J Reprod Fertil Suppl 54, 385–399.Google Scholar
Wallace, JM, Bourke, DA, Aitken, RP & Cruickshank, MA (1999b) Switching maternal dietary intake at the end of the first trimester has profound effects on placental development and foetal growth in adolescent ewes carrying singleton fetuses. Biol Reprod 61, 101–110.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, 100–108.Google Scholar
Wallace, JM, Bourke, DA, Da Silva, P & Aitken, RP (2001) Nutrient partitioning during adolescent pregnancy. Reproduction 122, 347–357.Google Scholar
Wallace, JM, Bourke, DA, Aitken, RP, Leitch, N & Hay, WW Jr (2002a) (2002 a ) Blood flows and nutrient uptakes in growth-restricted pregnancies induced by overnourishing adolescent sheep. Am J Physiol Regul Integr Comp Physiol 282, R1027–R1036.Google Scholar
Wallace, JM, Bourke, DA, Aitken, RP, Milne, RA, Milne, JS & Hay, WW Jr (2002b) Placental glucose transport in growth-restricted pregnancies induced by overnourishing adolescent sheep. J Physiol 547, 85–94.Google Scholar
Wallace, JM, Aitken, RP, Milne, JS & Hay, WW Jr (2004a) Nutritionally-mediated placental growth restriction in the growing adolescent: consequences for the fetus. Biol Reprod 71, 1055–1062.Google Scholar
Wallace, JM, Milne, JS & Aitken, RP (2004 b) Maternal growth hormone treatment from day 35 to 80 of gestation alters nutrient partitioning in favour of uteroplacental growth in the overnourished adolescent sheep. Biol Reprod 70, 1277–1285.Google Scholar
Williams, AH & Cumming, IA (1982) Inverse relationship between concentrations of progesterone and nutrition in ewes. J Agric Sci 98, 517–522.Google Scholar