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Influence of maternal pre-pregnancy body composition and diet during early–mid pregnancy on cardiovascular function and nephron number in juvenile sheep

Published online by Cambridge University Press:  08 March 2007

G. S. Gopalakrishnan ,
D. S. Gardner ,
J. Dandrea ,
S. C. Langley-Evans ,
S. Pearce ,
L. O. Kurlak ,
R. M. Walker ,
I. W. Seetho ,
D. H. Keisler  and
M. M. Ramsay
...Show all authors
G. S. Gopalakrishnan
Affiliation:
Centre for Reproduction and Early Life, Institute of Clinical Research, University Hospital, Nottingham NG7 2UH, UK
D. S. Gardner*
Affiliation:
Centre for Reproduction and Early Life, Institute of Clinical Research, University Hospital, Nottingham NG7 2UH, UK
J. Dandrea
Affiliation:
Centre for Reproduction and Early Life, Institute of Clinical Research, University Hospital, Nottingham NG7 2UH, UK
S. C. Langley-Evans
Affiliation:
School of Biosciences, University of Nottingham, Sutton Bonington Campus, Nottingham, UK
S. Pearce
Affiliation:
Centre for Reproduction and Early Life, Institute of Clinical Research, University Hospital, Nottingham NG7 2UH, UK
L. O. Kurlak
Affiliation:
Centre for Reproduction and Early Life, Institute of Clinical Research, University Hospital, Nottingham NG7 2UH, UK
R. M. Walker
Affiliation:
School of Biosciences, University of Nottingham, Sutton Bonington Campus, Nottingham, UK
I. W. Seetho
Affiliation:
Centre for Reproduction and Early Life, Institute of Clinical Research, University Hospital, Nottingham NG7 2UH, UK
D. H. Keisler
Affiliation:
Department of Animal Sciences, University of Missouri, Columbia, MO 65201, USA
M. M. Ramsay
Affiliation:
Centre for Reproduction and Early Life, Institute of Clinical Research, University Hospital, Nottingham NG7 2UH, UK
T. Stephenson
Affiliation:
Centre for Reproduction and Early Life, Institute of Clinical Research, University Hospital, Nottingham NG7 2UH, UK
M. E. Symonds
Affiliation:
Centre for Reproduction and Early Life, Institute of Clinical Research, University Hospital, Nottingham NG7 2UH, UK
*
*Corresponding author: Dr David S. Gardner, fax +44 115 970 9382, email david.gardner@nottingham.ac.uk
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Abstract

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The prenatal diet can program an individual's cardiovascular system towards later higher resting blood pressure and kidney dysfunction, but the extent to which these programmed responses are directly determined by the timing of maternal nutritional manipulation is unknown. In the present study we examined whether maternal nutrient restriction targeted over the period of maximal placental growth, i.e. days 28–80 of gestation, resulted in altered blood pressure or kidney development in the juvenile offspring. This was undertaken in 6-month-old sheep born to mothers fed control (100–150 % of the recommended metabolisable energy (ME) intake for that stage of gestation) or nutrient-restricted (NR; 50 % ME; n 6) diets between days 28 and 80 of gestation. Controls were additionally grouped according to normal (>3, n 7) or low body condition score (LBCS; <2, n 6), thereby enabling us to examine the effect of maternal body composition on later cardiovascular function. From day 80 to term (approximately 147 d) all sheep were fed to 100 % ME. Offspring were weaned at 12 weeks and pasture-reared until 6 months of age when cardiovascular function was determined. Both LBCS and NR sheep tended to have lower resting systolic (control, 85 (SE 2); LBCS, 77 (SE 3); NR, 77 (SE 3) mmHg) and diastolic blood pressure relative to controls. Total nephron count was markedly lower in both LBCS and NR relative to controls (LBCS, 59 (SE 6); NR, 56 (SE 12) %). Our data suggest that maternal body composition around conception is as important as the level of nutrient intake during early pregnancy in programming later cardiovascular health.

Keywords

ProgrammingNutritionNephronBlood pressure
Type
Research Article
Information
British Journal of Nutrition , Volume 94 , Issue 6 , December 2005 , pp. 938 - 947
Copyright
Copyright © The Nutrition Society 2005

References

Agricultural and Food Research Council (1993) Technical Committee on Responses to Nutrients Report no. 9, pp. 812–815. Wallingford, UK: CAB International.Google Scholar
Agricultural Research Council (1980) Requirements for energy. In The Nutritional Requirements of Ruminant Livestock, pp. 115–119. Slough, UK: Commonwealth Agricultural Bureau.Google Scholar
Barker, DJP (2001) The malnourished baby and infant. Br Med Bull 60, 69–88.CrossRefGoogle ScholarPubMed
Barker, DJP, Bull, AR, Osmond, C & Simmonds, SJ (1990) Fetal and placental size and risk of hypertension in adult life. Br Med J 301, 259–262.CrossRefGoogle ScholarPubMed
Barker, DJP, Gluckman, PD, Godfrey, KM, Harding, JE, Owens, JA & Robinson, JS (1993) Fetal nutrition and cardiovascular disease in later life. Lancet 341, 938–941.CrossRefGoogle Scholar
Bispham, J, Gopalakrishnan, GS, Dandrea, J, Wilson, V, Budge, H, Keisler, DHBroughton Pipkin, F, Stephenson, T & Symonds, ME (2003) Maternal endocrine adaptation throughout pregnancy to nutritional manipulation: consequences for maternal plasma leptin and cortisol and the programming of fetal adipose tissue development. Endocrinology 144, 3575–3585.CrossRefGoogle ScholarPubMed
Brennan, KA, Gopalakrishnan, GS, Kurlak, L, Rhind, SM, Brooks, AN, Rae, MT, Olson, DM, Stephenson, T & Symonds, ME (2005) Impact of maternal undernutrition and fetal number on glucocorticoid, growth hormone and insulin-like growth factor receptor mRNA abundance in the ovine fetal kidney. Reproduction 129, 151–159.CrossRefGoogle ScholarPubMed
Clarke, L, Heasman, L, Juniper, DT & Symonds, ME (1998) Maternal nutrition in early–mid gestation and placental size in sheep. Br J Nutr 79, 359–364.CrossRefGoogle ScholarPubMed
Clarke, L, Yakubu, DP & Symonds, ME (1997) Influence of maternal bodyweight on size, conformation and survival of newborn lambs. Reprod Fertil Dev 9, 509–514.CrossRefGoogle ScholarPubMed
Crowe, C, Dandekar, P, Fox, M, Dhingra, K, Bennet, L & Hanson, MA (1995) The effects of anaemia on heart, placenta and body weight, and blood pressure in fetal and neonatal rats. J Physiol 488, 515–519.CrossRefGoogle ScholarPubMed
Delavaud, C, Bocquier, F, Chilliard, Y, Keisler, DH, Gertler, A & Kann, G (2000) Effect of sheep nutritional status and body fatness on plasma leptin concentration assessed by a specific RIA. J Endocrinol 165, 519–526.CrossRefGoogle ScholarPubMed
Dodic, M, Hantzis, V, Duncan, J, Rees, S, Koukoulas, I, Johnson, K, Wintour, EM & Moritz, K (2002) Programming effects of short prenatal exposure to cortisol. FASEB J 16, 1017–1026.CrossRefGoogle ScholarPubMed
Eckberg, DL (1979) Carotid baroreflex function in young men with borderline blood pressure elevation. Circulation 59, 632–636.CrossRefGoogle ScholarPubMed
Edwards, LJ & McMillen, IC (2002) Impact of maternal undernutrition during the periconceptional period, fetal number, and fetal sex on the development of the hypothalamo-pituitary adrenal axis in sheep during late gestation. Biol Reprod 66, 1562–1569.CrossRefGoogle ScholarPubMed
Gambling, L, Dunford, S, Wallace, DI, Zuur, G, Solanky, N, Srai, KS & McArdle, HJ (2003) Iron deficiency during pregnancy affects postnatal blood pressure in the rat. J Physiol 552, 603–610.CrossRefGoogle ScholarPubMed
Gardner, DS, Jamall, E, Fletcher, AJW, Fowden, AL & Giussani, DA (2004a) Adrenocortical responsiveness is blunted in twin relative to singleton ovine fetuses. J Physiol 557, 1021–1032.CrossRefGoogle ScholarPubMed
Gardner, DS, Pearce, S, Dandrea, J, Walker, RM, Ramsey, MM, Stephenson, T & Symonds, ME (2004b) Peri-implantation undernutrition programs blunted angiotensin II evoked baroreflex responses in young adult sheep. Hypertension 43, 1–7.CrossRefGoogle ScholarPubMed
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. J Physiol 565, 137–148.CrossRefGoogle ScholarPubMed
Gopalakrishnan, GS, Gardner, DS, Kurlak, L, Langley-Evans, SC, Rhind, SM, Rae, MT, Kyle, CE, Stephenson, T, Symonds, ME & Budge, H (2004a) Programming of nephron number in adult sheep by maternal nutrient restriction in early gestation. Proc Physiol Soc 560, C18.Google Scholar
Gopalakrishnan, G, Gardner, DS & Rhind, SM (2004b) Programming of adult cardiovascular function after early maternal undernutrition in sheep. Am J Physiol 287, R12–R20.Google ScholarPubMed
Hawkins, P, Steyn, C, McGarrigle, HG, 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. Reprod Fertil Dev 12, 443–456.CrossRefGoogle 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. Pediatr Res 44, 546–551.CrossRefGoogle ScholarPubMed
Jackson, AA, Dunn, RL, Marchand, MC & Langley-Evans, SC (2002) Increased systolic blood pressure in rats induced by a maternal low-protein diet is reversed by dietary supplementation with glycine. Clin Sci 103, 633–639.CrossRefGoogle ScholarPubMed
Langley, SC & Jackson, AA (1994) Increased systolic blood pressure in adult rats induced by fetal exposure to maternal low protein diet. Clin Sci 86, 217–222.CrossRefGoogle Scholar
Langley-Evans, SC (2001) Fetal programming of cardiovascular function through exposure to maternal undernutrition. Proc Nutr Soc 60, 505–513.CrossRefGoogle ScholarPubMed
Langley-Evans, SC, Welham, SJM & Jackson, AA (1999) Fetal exposure to a maternal low protein diet impairs nephrogenesis and promotes hypertension in the rat. Life Sci 64, 965–974.CrossRefGoogle ScholarPubMed
Mackenzie, HS & Brenner, BM (1995) Fewer nephrons at birth: a missing link in the etiology of essential hypertension? Am J Kidney Dis 91, 98.Google Scholar
McMullen, S & Langley-Evans, SC (2004) Maternal low protein diet in rat pregnancy programmes blood pressure through sex-specific mechanisms. Am J Physiol 288, R85–R90.Google ScholarPubMed
Matthews, JN, Altman, DG, Campbell, MJ & Royston, P (1990) Analysis of serial measurements in medical research. Br Med J 300, 230–235.CrossRefGoogle ScholarPubMed
Mostyn, A, Wilson, V, Dandrea, J, Yakubu, DP, Budge, H, Alves-Guerra, MC, Pecqueur, C, Miroux, B, Symonds, ME & Stephenson, T (2003) Ontogeny and nutritional manipulation of mitochondrial protein abundance in adipose tissue and the lungs of postnatal sheep. Br J Nutr 90, 323–328.CrossRefGoogle ScholarPubMed
Ookuwa, H, Takata, S, Ogawa, J, Iwase, N, Ikeda, T & Hattori, N (1987) Abnormal cardiopulmonary baroreflexes in normotensive young subjects with a family history of essential hypertension. J Clin Hypertens 3, 596–604.Google ScholarPubMed
Ozaki, T, Nishina, H, Hanson, MA & Poston, L (2001) Dietary restriction in pregnant rats causes gender-related hypertension and vascular dysfunction in offspring. J Physiol 530, 141–152.CrossRefGoogle ScholarPubMed
Robinson, JS, Owens, JA, DeBarro, T, Lok, F & Chidzanja, S (1994) Maternal nutrition and fetal growth. In Early Fetal Growth and Development, pp. 317–329 [Ward, RHT, Smith, SK and Donnai, D, editors]. London: RCOG Press.Google Scholar
Russel, AJF, Doney, JM & Gunn, RG (1969) Subjective assessment of body fat in live sheep. J Agric Sci (Cambridge) 72, 451–454.CrossRefGoogle Scholar
Schwartz, J & Rose, JC (1998) Development of the pituitary adrenal axis in fetal sheep twins. Am J Physiol 274, R1–R8.Google ScholarPubMed
Smith, FG, Chan, S & De Wildt, SN (1997) Effects of renal denervation on cardiovascular and renal responses to ACE inhibition in conscious lambs. J Appl Physiol 83, 414–419.CrossRefGoogle ScholarPubMed
Symonds, ME, Bryant, MJ, Clarke, L, Darby, CJ & Lomax, MA (1992) Effect of maternal cold exposure on brown adipose tissue and thermogenesis in the neonatal lamb. J Physiol 455, 487–502.CrossRefGoogle ScholarPubMed
Symonds, ME, Bryant, MJ & Lomax, MA (1986) The effect of shearing on the energy metabolism of the pregnant ewe. Br J Nutr 56, 635–643.CrossRefGoogle ScholarPubMed
Wallace, JM (2000) Nutrient partitioning during pregnancy: adverse gestational outcome in overnourished adolescent dams. Proc Nutr Soc 59, 107–117.CrossRefGoogle ScholarPubMed
Wallace, JM, Aitken, RP & Cheyne, MA (1996) Nutrient partitioning and fetal growth in rapidly growing adolescent ewes. J Reprod Fertil 107, 183–190.CrossRefGoogle ScholarPubMed
Wallace, JM, Bourke, DA, Aitken, RP, Milne, JS & Hay, WW (2003) Placental glucose transport in growth-restricted pregnancies induced by overnourishing adolescent sheep. J Physiol 547, 85–94.CrossRefGoogle ScholarPubMed
Welham, SJM, Wade, A & Woolf, AS (2002) Protein restriction in pregnancy is associated with increased apoptosis of mesenchymal cells at the start of rat metanephrogenesis. Kidney Int 61, 1231–1242.CrossRefGoogle ScholarPubMed
Whorwood, CB, Firth, KM, Budge, H & Symonds, ME (2001) Maternal undernutrition during early- to mid-gestation programmes tissue-specific alterations in the expression of the glucocorticoid receptor, 11β-hydroxysteroid dehydrogenase isoforms and type 1 angiotensin II receptor in neonatal sheep. Endocrinology 142, 2854–2864.CrossRefGoogle Scholar
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. J Physiol 549, 929–935.CrossRefGoogle ScholarPubMed
Woods, LL, Ingelfinger, JR, Nyengaard, JR & Rasch, R (2001) Maternal protein restriction suppresses the newborn rennin–angiotensin system and programs adult hypertension in rats. Pediatr Res 49, 460–467.CrossRefGoogle Scholar
Yang, K, Berdusco, ET & Challis, JR (1994) Opposite effects of glucocorticoid on hepatic 11×-hydroxysteroid dehydrogenase mRNA and activity in fetal and adult sheep. J Endocrinol 143, 121–126.CrossRefGoogle ScholarPubMed