Table of Contents Author Guidelines Submit a Manuscript
Journal of Pregnancy
Volume 2011, Article ID 740408, 9 pages
http://dx.doi.org/10.1155/2011/740408
Review Article

Catecholamines Mediate Multiple Fetal Adaptations during Placental Insufficiency That Contribute to Intrauterine Growth Restriction: Lessons from Hyperthermic Sheep

Department of Animal Sciences, The University of Arizona, 1650 E. Limberlost Drive, Tucson, AZ 85719, USA

Received 12 January 2011; Accepted 11 March 2011

Academic Editor: R. L. Deter

Copyright © 2011 D. T. Yates et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. K. Creasy, R. Resnik, and J. Iams, Maternal-Fetal Medicine: Principles and Practice, Saunders, Philadelphia, Pa, USA, 2004.
  2. E. Platz and R. Newman, “Diagnosis of IUGR: traditional Biometry,” Seminars in Perinatology, vol. 32, no. 3, pp. 140–147, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  3. D. L. Economides, K. H. Nicolaides, W. A. Gahl, I. Bernardini, and M. I. Evans, “Plasma amino acids in appropriate- and small-for-gestational-age fetuses,” American Journal of Obstetrics and Gynecology, vol. 161, no. 5, pp. 1219–1227, 1989. View at Google Scholar · View at Scopus
  4. S. Setia, M. G. Sridhar, V. Bhat, L. Chaturvedula, R. Vinayagamoorti, and M. John, “Insulin sensitivity and insulin secretion at birth in intrauterine growth retarded infants,” Pathology, vol. 38, no. 3, pp. 236–238, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  5. D. L. Economides, A. Proudler, and K. H. Nicolaides, “Plasma insulin in appropriate- and small-for-gestational-age fetuses,” American Journal of Obstetrics and Gynecology, vol. 160, no. 5, pp. 1091–1094, 1989. View at Google Scholar · View at Scopus
  6. A. Greenough, K. H. Nicolaides, and H. Lagercrantz, “Human fetal sympathoadrenal responsiveness,” Early Human Development, vol. 23, no. 1, pp. 9–13, 1990. View at Google Scholar · View at Scopus
  7. K. Okamura, T. Watanabe, S. Tanigawara et al., “Catecholamine levels and their correlation to blood gases in umbilical venous blood obtained by cordocentesis,” Fetal Diagnosis and Therapy, vol. 5, no. 3-4, pp. 147–152, 1990. View at Google Scholar · View at Scopus
  8. J. S. Barry, P. J. Rozance, and R. V. Anthony, “An animal model of placental insufficiency-induced intrauterine growth restriction,” Seminars in Perinatology, vol. 32, no. 3, pp. 225–230, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  9. B. De Vrijer, M. L. Davidsen, R. B. Wilkening, R. V. Anthony, and T. R. H. Regnault, “Altered placental and fetal expression of IGFS and IGF-binding proteins associated with intrauterine growth restriction in fetal sheep during early and mid-pregnancy,” Pediatric Research, vol. 60, no. 5, pp. 507–512, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  10. T. R. H. Regnault, H. L. Galan, T. A. Parker, and R. V. Anthony, “Placental development in normal and compromised pregnancies—a review,” Placenta, vol. 23, supplement A, pp. S119–S129, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  11. T. R. H. Regnault, B. de Vrijer, H. L. Galan, R. B. Wilkening, F. C. Battaglia, and G. Meschia, “Development and mechanisms of fetal hypoxia in severe fetal growth restriction,” Placenta, vol. 28, no. 7, pp. 714–723, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  12. M. H. Vickers, B. H. Breier, W. S. Cutfield, P. L. Hofman, and P. D. Gluckman, “Fetal origins of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition,” American Journal of Physiology, vol. 279, no. 1, pp. E83–E87, 2000. View at Google Scholar · View at Scopus
  13. M. Desai, D. Gayle, J. Babu, and M. G. Ross, “Programmed obesity in intrauterine growth-restricted newborns: modulation by newborn nutrition,” American Journal of Physiology, vol. 288, no. 1, pp. R91–R96, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  14. D. J. P. Barker, C. N. Hales, C. H. D. Fall, C. Osmond, K. Phipps, and P. M. S. Clark, “Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth,” Diabetologia, vol. 36, no. 1, pp. 62–67, 1993. View at Publisher · View at Google Scholar · View at Scopus
  15. A. C. J. Ravelli, J. H. P. Van Der Meulen, R. P. J. Michels et al., “Glucose tolerance in adults after prenatal exposure to famine,” Lancet, vol. 351, no. 9097, pp. 173–177, 1998. View at Publisher · View at Google Scholar · View at Scopus
  16. C. A. Newsome, A. W. Shiell, C. H. D. Fall, D. I. W. Phillips, R. Shier, and C. M. Law, “Is birth weight related to later glucose and insulin metabolism?—a systematic review,” Diabetic Medicine, vol. 20, no. 5, pp. 339–348, 2003. View at Publisher · View at Google Scholar · View at Scopus
  17. A. S. Green, P. J. Rozance, and S. W. Limesand, “Consequences of a compromised intrauterine environment on islet function,” Journal of Endocrinology, vol. 205, no. 3, pp. 211–224, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  18. H. L. Galan, M. J. Hussey, A. Barbera et al., “Relationship of fetal growth to duration of heat stress in an ovine model of placental insufficiency,” American Journal of Obstetrics and Gynecology, vol. 180, no. 5, pp. 1278–1282, 1999. View at Publisher · View at Google Scholar · View at Scopus
  19. C. E. Dreiling, F. S. Carman 3rd. F.S., and D. E. Brown, “Maternal endocrine and fetal metabolic responses to heat stress,” Journal of Dairy Science, vol. 74, no. 1, pp. 312–327, 1991. View at Google Scholar · View at Scopus
  20. T. R. H. Regnault, R. J. Orbus, F. C. Battaglia, R. B. Wilkening, and R. V. Anthony, “Altered arterial concentrations of placental hormones during maximal placental growth in a model of placental insufficiency,” Journal of Endocrinology, vol. 162, no. 3, pp. 433–442, 1999. View at Publisher · View at Google Scholar · View at Scopus
  21. J. C. K. Wells, “Thermal environment and human birth weight,” Journal of Theoretical Biology, vol. 214, no. 3, pp. 413–425, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  22. G. Alexander and D. Williams, “Heat stress and development of conceptus in domestic sheep,” Journal of Agricultural Science, vol. 76, pp. 53–72, 1971. View at Google Scholar
  23. P. J. Thureen, K. A. Trembler, G. Meschia, E. L. Makowski, and R. B. Wilkening, “Placental glucose transport in heat-induced fetal growth retardation,” American Journal of Physiology, vol. 263, no. 3, pp. R578–R585, 1992. View at Google Scholar · View at Scopus
  24. T. R. H. Regnault, R. J. Orbus, B. De Vrijer et al., “Placental expression of VEGF, PlGF and their receptors in a model of placental insufficiency—intrauterine growth restriction (PI-IUGR),” Placenta, vol. 23, no. 2-3, pp. 132–144, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  25. J. A. Arroyo and V. D. Winn, “Vasculogenesis and angiogenesis in the IUGR placenta,” Seminars in Perinatology, vol. 32, no. 3, pp. 172–177, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  26. L. P. Reynolds, P. P. Borowicz, K. A. Vonnahme et al., “Animal models of placental angiogenesis,” Placenta, vol. 26, no. 10, pp. 689–708, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  27. F. Lyall, A. Young, F. Boswell, J. C. P. Kingdom, and I. A. Greer, “Placental expression of vascular endothelial growth factor in placentae from pregnancies complicated by pre-eclampsia and intrauterine growth restriction does not support placental hypoxia at delivery,” Placenta, vol. 18, no. 4, pp. 269–276, 1997. View at Publisher · View at Google Scholar · View at Scopus
  28. J. Kingdom, B. Huppertz, G. Seaward, and P. Kaufmann, “Development of the placental villous tree and its consequences for fetal growth,” European Journal of Obstetrics Gynecology and Reproductive Biology, vol. 92, no. 1, pp. 35–43, 2000. View at Publisher · View at Google Scholar · View at Scopus
  29. J. C. P. Kingdom and P. Kaufmann, “Oxygen and placental villous development: origins of fetal hypoxia,” Placenta, vol. 18, no. 8, pp. 613–621, 1997. View at Publisher · View at Google Scholar · View at Scopus
  30. S. W. Limesand, T. R. H. Regnault, and W. W. Hay, “Characterization of glucose transporter 8 (GLUT8) in the ovine placenta of normal and growth restricted fetuses,” Placenta, vol. 25, no. 1, pp. 70–77, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  31. S. W. Limesand, P. J. Rozance, D. Smith, and W. W. Hay, “Increased insulin sensitivity and maintenance of glucose utilization rates in fetal sheep with placental insufficiency and intrauterine growth restriction,” American Journal of Physiology, vol. 293, no. 6, pp. E1716–E1725, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  32. B. De Vrijer, T. R. H. Regnault, R. B. Wilkening, G. Meschia, and F. C. Battaglia, “Placental uptake and transport of ACP, a neutral nonmetabolizable amino acid, in an ovine model of fetal growth restriction,” American Journal of Physiology, vol. 287, no. 6, pp. E1114–E1124, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  33. J. M. Wallace, T. R. H. Regnault, S. W. Limesand, W. W. Hay, and R. V. Anthony, “Investigating the causes of low birth weight in contrasting ovine paradigms,” Journal of Physiology, vol. 565, no. 1, pp. 19–26, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  34. A. W. Bell, R. B. Wilkening, and G. Meschia, “Some aspects of placental function in chronically heat-stressed ewes,” Journal of Developmental Physiology, vol. 9, no. 1, pp. 17–29, 1987. View at Google Scholar · View at Scopus
  35. R. A. Ehrhardt and A. W. Bell, “Developmental increases in glucose transporter concentration in the sheep placenta,” American Journal of Physiology, vol. 273, no. 3, pp. R1132–R1141, 1997. View at Google Scholar · View at Scopus
  36. F. B. P. Wooding, A. L. Fowden, A. W. Bell, R. A. Ehrhardt, S. W. Limesand, and W. W. Hay, “Localisation of glucose transport in the ruminant placenta: implications for sequential use of transporter isoforms,” Placenta, vol. 26, no. 8-9, pp. 626–640, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  37. A. H. Anderson, P. V. Fennessey, G. Meschia, R. B. Wilkening, and F. C. Battaglia, “Placental transport of threonine and its utilization in the normal and growth-restricted fetus,” American Journal of Physiology, vol. 272, no. 5, pp. E892–E900, 1997. View at Google Scholar · View at Scopus
  38. J. C. Ross, P. V. Fennessey, R. B. Wilkening, F. C. Battaglia, and G. Meschia, “Placental transport and fetal utilization of leucine in a model of fetal growth retardation,” American Journal of Physiology, vol. 270, no. 3, pp. E491–E503, 1996. View at Google Scholar · View at Scopus
  39. T. R. H. Regnault, B. De Vrijer, and F. C. Battaglia, “Transport and metabolism of amino acids in placenta,” Endocrine, vol. 19, no. 1, pp. 23–41, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  40. M. S. Malandro, M. J. Beveridge, D. A. Novak, and M. S. Kilberg, “Rat placental amino acid transport after protein-deprivation-induced intrauterine growth retardation,” Biochemical Society Transactions, vol. 24, no. 3, pp. 839–843, 1996. View at Google Scholar · View at Scopus
  41. P. Rosso, “Maternal-fetal exchange during protein malnutrition in the rat. Placental transfer of glucose and a nonmetabolizable glucose analog,” Journal of Nutrition, vol. 107, no. 11, pp. 20006–20010, 1977. View at Google Scholar · View at Scopus
  42. R. A. Leos, M. J. Anderson, X. Chen, J. Pugmire, K. A. Anderson, and S. W. Limesand, “Chronic exposure to elevated norepinephrine suppresses insulin secretion in fetal sheep with placental insufficiency and intrauterine growth restriction,” American Journal of Physiology, vol. 298, no. 4, pp. E770–E778, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  43. C. N. Hales and D. J. P. Barker, “Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis,” Diabetologia, vol. 35, no. 7, pp. 595–601, 1992. View at Publisher · View at Google Scholar · View at Scopus
  44. C. N. Hales and D. J. P. Barker, “The thrifty phenotype hypothesis,” British Medical Bulletin, vol. 60, pp. 5–20, 2001. View at Publisher · View at Google Scholar · View at Scopus
  45. J. K. Jellyman, D. S. Gardner, C. M. B. Edwards, A. L. Fowden, and D. A. Giussani, “Fetal cardiovascular, metabolic and endocrine responses to acute hypoxaemia during and following maternal treatment with dexamethasone in sheep,” Journal of Physiology, vol. 567, no. 2, pp. 673–688, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  46. M. B. Adams and I. C. McMillen, “Actions of hypoxia on catecholamine synthetic enzyme mRNA expression before and after development of adrenal innervation in the sheep fetus,” Journal of Physiology, vol. 529, no. 3, pp. 519–531, 2000. View at Publisher · View at Google Scholar · View at Scopus
  47. R. S. Comline and M. Silver, “Development of activity in the adrenal medulla of the foetus and new-born animal,” British Medical Bulletin, vol. 22, no. 1, pp. 16–20, 1966. View at Google Scholar · View at Scopus
  48. C. T. Jones and R. O. Robinson, “Plasma catecholamines in foetal and adult sheep,” Journal of Physiology, vol. 248, no. 1, pp. 15–33, 1975. View at Google Scholar · View at Scopus
  49. C. Y. Cheung, “Fetal adrenal medulla catecholamine response to hypoxia-direct and neural components,” American Journal of Physiology, vol. 258, no. 6, pp. R1340–R1346, 1990. View at Google Scholar · View at Scopus
  50. W. R. Cohen, G. J. Piasecki, H. E. Cohn, J. B. Susa, and B. T. Jackson, “Sympathoadrenal responses during hypoglycemia, hyperinsulinemia, and hypoxemia in the ovine fetus,” American Journal of Physiology, vol. 261, no. 1, pp. E95–E102, 1991. View at Google Scholar · View at Scopus
  51. R. S. Comline and M. Silver, “The release of adrenaline and noradrenaline from the adrenal glands of the foetal sheep,” The Journal of Physiology, vol. 156, pp. 424–444, 1961. View at Google Scholar · View at Scopus
  52. T. Maeda and B. J. Koos, “Adenosine A1 and A2a receptors modulate insulinemia, glycemia, and lactatemia in fetal sheep,” American Journal of Physiology, vol. 296, no. 3, pp. R693–R701, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  53. B. J. Koos and T. Maeda, “Adenosine A2A receptors mediate cardiovascular responses to hypoxia in fetal sheep,” American Journal of Physiology, vol. 280, no. 1, pp. H83–H89, 2001. View at Google Scholar · View at Scopus
  54. P. J. Rozance, S. W. Limesand, J. S. Barry et al., “Chronic late-gestation hypoglycemia upregulates hepatic PEPCK associated with increased PGC1α mRNA and phosphorylated CREB in fetal sheep,” American Journal of Physiology, vol. 294, no. 2, pp. E365–E370, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  55. S. W. Limesand and W. W. Hay, “Adaptation of ovine fetal pancreatic insulin secretion to chronic hypoglycaemia and euglycaemic correction,” Journal of Physiology, vol. 547, no. 1, pp. 95–105, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  56. S. W. Limesand, P. J. Rozance, G. O. Zerbe, J. C. Hutton, and W. W. Hay, “Attenuated insulin release and storage in fetal sheep pancreatic islets with intrauterine growth restriction,” Endocrinology, vol. 147, no. 3, pp. 1488–1497, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  57. X. Chen, A. L. Fahy, A. S. Green, M. J. Anderson, R. P. Rhoads, and S. W. Limesand, “β2-adrenergic receptor desensitization in perirenal adipose tissue in fetuses and lambs with placental insufficiency-induced intrauterine growth restriction,” Journal of Physiology, vol. 588, no. 18, pp. 3539–3549, 2010. View at Publisher · View at Google Scholar · View at PubMed
  58. V. Mericq, K. K. Ong, R. Bazaes et al., “Longitudinal changes in insulin sensitivity and secretion from birth to age three years in small- and appropriate-for-gestational-age children,” Diabetologia, vol. 48, no. 12, pp. 2609–2614, 2005. View at Publisher · View at Google Scholar · View at PubMed
  59. N. Soto, R. A. Bazaes, V. Peña et al., “Insulin sensitivity and secretion are related to catch-up growth in small-for-gestational-age infants at age 1 year: results from a prospective cohort,” Journal of Clinical Endocrinology and Metabolism, vol. 88, no. 8, pp. 3645–3650, 2003. View at Publisher · View at Google Scholar
  60. S. Johansson, M. Norman, L. Legnevall, Y. Dalmaz, H. Lagercrantz, and M. Vanpée, “Increased catecholamines and heart rate in children with low birth weight: perinatal contributions to sympathoadrenal overactivity,” Journal of Internal Medicine, vol. 261, no. 5, pp. 480–487, 2007. View at Publisher · View at Google Scholar · View at PubMed
  61. A. A. M. W. van Kempen, M. T. Ackermans, E. Endert, J. H. Kok, and H. P. Sauerwein, “Glucose production in response to glucagon is comparable in preterm AGA and SGA infants,” Clinical Nutrition, vol. 24, no. 5, pp. 727–736, 2005. View at Publisher · View at Google Scholar · View at PubMed
  62. T. Strinic, D. Roje, J. Marusic, and V. Capkun, “Cord blood cortisol level is lower in growth-restricted newborns,” Journal of Obstetrics and Gynaecology Research, vol. 33, no. 2, pp. 144–150, 2007. View at Publisher · View at Google Scholar · View at PubMed
  63. L. C. Giudice, F. De Zegher, S. E. Gargosky et al., “Insulin-like growth factors and their binding proteins in the term and preterm human fetus and neonate with normal and extremes of intrauterine growth,” Journal of Clinical Endocrinology and Metabolism, vol. 80, no. 5, pp. 1548–1555, 1995. View at Google Scholar
  64. C. A. Jefferies, P. L. Hofman, J. A. Keelan, E. A. Robinson, and W. S. Cutfield, “Insulin resistance is not due to persistently elevated serum tumor necrosis-α levels in small for gestational age, premature, or twin children,” Pediatric Diabetes, vol. 5, no. 1, pp. 20–25, 2004. View at Publisher · View at Google Scholar · View at PubMed
  65. C. Hubinont, U. Nicolini, N. M. Fisk, Y. Tannirandorn, and C. H. Rodeck, “Endocrine pancreatic function in growth-retarded fetuses,” Obstetrics and Gynecology, vol. 77, no. 4, pp. 541–544, 1991. View at Google Scholar
  66. B. A. Chappell, J. F. Padbury, D. M. Habib et al., “Pulmonary clearance of norepinephrine in lambs,” Pediatric Research, vol. 29, no. 1, pp. 93–97, 1991. View at Google Scholar
  67. S. Louey, M. L. Cock, K. M. Stevenson, and R. Harding, “Placental insufficiency and fetal growth restriction lead to postnatal hypotension and altered postnatal growth in sheep,” Pediatric Research, vol. 48, no. 6, pp. 808–814, 2000. View at Google Scholar
  68. L. A. Wallin, C. P. Fawcett, and C. R. Rosenfeld, “Oxytocin stimulates glucagon and insulin secretion in fetal and neonatal sheep,” Endocrinology, vol. 125, no. 5, pp. 2289–2296, 1989. View at Google Scholar
  69. H. F. Sadiq, U. G. Das, T. F. Tracy, and S. U. Devaskar, “Intra-uterine growth restriction differentially regulates perinatal brain and skeletal muscle glucose transporters,” Brain Research, vol. 823, no. 1-2, pp. 96–103, 1999. View at Publisher · View at Google Scholar
  70. U. G. Das, R. E. Schroeder, W. W. Hay, and S. U. Devaskar, “Time-dependent and tissue-specific effects of circulating glucose on fetal ovine glucose transporters,” American Journal of Physiology, vol. 276, no. 3, pp. R809–R817, 1999. View at Google Scholar
  71. S. R. Thorn, T. R. H. Regnault, L. D. Brown et al., “Intrauterine growth restriction increases fetal hepatic gluconeogenic capacity and reduces messenger ribonucleic acid translation initiation and nutrient sensing in fetal liver and skeletal muscle,” Endocrinology, vol. 150, no. 7, pp. 3021–3030, 2009. View at Publisher · View at Google Scholar · View at PubMed
  72. S. W. Limesand, P. J. Rozance, L. D. Brown, and W. W. Hay, “Effects of chronic hypoglycemia and euglycemic correction on lysine metabolism in fetal sheep,” American Journal of Physiology, vol. 296, no. 4, pp. E879–E887, 2009. View at Publisher · View at Google Scholar · View at PubMed
  73. F. C. Battaglia and G. Meschia, “Principal substrates of fetal metabolism,” Physiological Reviews, vol. 58, no. 2, pp. 499–527, 1978. View at Google Scholar
  74. C. T. Jones and J. W. K. Ritchie, “The metabolic and endocrine effects of circulating catecholamines in fetal sheep,” Journal of Physiology, vol. 285, pp. 395–408, 1978. View at Google Scholar
  75. J. S. Barry, M. L. Davidsen, S. W. Limesand et al., “Developmental changes in ovine myocardial glucose transporters and insulin signaling following hyperthermia-induced intrauterine fetal growth restriction,” Experimental Biology and Medicine, vol. 231, no. 5, pp. 566–575, 2006. View at Google Scholar
  76. W. W. Hay, J. E. DiGiacomo, H. K. Meznarich, K. Hirst, and G. Zerbe, “Effects of glucose and insulin on fetal glucose oxidation and oxygen consumption,” American Journal of Physiology, vol. 256, no. 6, pp. E704–E713, 1989. View at Google Scholar
  77. W. W. Hay, H. K. Meznarich, J. E. DiGiacomo, K. Hirst, and G. Zerbe, “Effects of insulin and glucose concentrations on glucose utilization in fetal sheep,” Pediatric Research, vol. 23, no. 4, pp. 381–387, 1988. View at Google Scholar
  78. A. L. Fowden, J. Mijovic, and M. Silver, “The effects of cortisol on hepatic and renal gluconeogenic enzyme activities in the sheep fetus during late gestation,” Journal of Endocrinology, vol. 137, no. 2, pp. 213–222, 1993. View at Google Scholar
  79. S. Gentili, J. L. Morrison, and I. C. McMillen, “Intrauterine growth restriction and differential patterns of hepatic growth and expression of IGF1, PCK2, and HSDL1 mRNA in the sheep fetus in late gestation,” Biology of Reproduction, vol. 80, no. 6, pp. 1121–1127, 2009. View at Publisher · View at Google Scholar · View at PubMed
  80. G. Alexander, J. R. S. Hales, D. Stevens, and J. B. Donelly, “Effects of acute and prolonged exposure to heat on regional blood flows in pregnant sheep,” Journal of Developmental Physiology, vol. 9, no. 1, pp. 1–15, 1987. View at Google Scholar
  81. D. W. Walker, J. R. Hale, A. A. Fawcett, and N. M. Pratt, “Cardiovascular responses to heat stress in late gestation fetal sheep,” Experimental Physiology, vol. 80, no. 5, pp. 755–766, 1995. View at Google Scholar
  82. H. L. Galan, R. V. Anthony, S. Rigano et al., “Fetal hypertension and abnormal Doppler velocimetry in an ovine model of intrauterine growth restriction,” American Journal of Obstetrics and Gynecology, vol. 192, no. 1, pp. 272–279, 2005. View at Publisher · View at Google Scholar · View at PubMed
  83. T. R. H. Regnault, B. de Vrijer, H. L. Galan et al., “The relationship between transplacental O2 diffusion and placental expression of PIGF, VEGF and their receptors in a placental insufficiency model of fetal growth restriction,” Journal of Physiology, vol. 550, no. 2, pp. 641–656, 2003. View at Publisher · View at Google Scholar · View at PubMed
  84. R. B. Wilkening, F. C. Battaglia, and G. Meschia, “The relationship of umbilical glucose uptake to uterine blood flow,” Journal of Developmental Physiology, vol. 7, no. 5, pp. 313–319, 1985. View at Google Scholar
  85. S. W. Limesand, J. Jensen, J. C. Hutton, and W. W. Hay, “Diminished β-cell replication contributes to reduced β-cell mass in fetal sheep with intrauterine growth restriction,” American Journal of Physiology, vol. 288, no. 5, pp. R1297–R1305, 2005. View at Publisher · View at Google Scholar · View at PubMed
  86. P. L. Greenwood, A. S. Hunt, J. W. Hermanson, and A. W. Bell, “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, vol. 76, no. 9, pp. 2354–2367, 1998. View at Google Scholar
  87. J. L. Morrison, J. A. Duffield, B. S. Muhlhausler, S. Gentili, and I. C. McMillen, “Fetal growth restriction, catch-up growth and the early origins of insulin resistance and visceral obesity,” Pediatric Nephrology, vol. 25, no. 4, pp. 669–677, 2010. View at Publisher · View at Google Scholar · View at PubMed