Maternal endocrine status in relation to pregnancy outcome in rapidly growing adolescent sheep

Jacqueline Wallace, P DaSilva, Raymond Aitken, Morven Cruickshank

Research output: Contribution to journalArticle

112 Citations (Scopus)

Abstract

It has previously been reported that high nutrient intakes which promote rapid maternal growth throughout pregnancy are associated with poor pregnancy outcome when compared with normally growing adolescent animals. The present study examined the maternal plasma concentrations of a number of putative endocrine regulators of nutrient partitioning between the maternal and fetal compartments in relation to placental and fetal growth in this novel experimental paradigm. Embryos were recovered on day 4 after oestrus fi-om superovulated adult ewes that had been inseminated using semen from a single sire and synchronously transferred, in singleton, to the uterus of peripubertal adolescent recipients (n=38), which had been induced to ovulate at 32 weeks of age Give weight 47.4+/-0.4 kg). Post-transfer, the adolescent recipients were offered a high (n=21) or moderate (n=17) level of a complete diet calculated to achieve rapid (RMG) or normal (NMG) maternal growth rates. After day 100 of gestation, the feed intake of the NMG group was adjusted weekly to meet the increasing nutrient demands of the gravid uterus. Pregnancy rate following embryo transfer was higher (P<0.05) in the RMG (90%) than in the NMG (59%) group. For ewes delivering live young at term, liveweight gain during the first 100 days of gestation was 294 +/- 12.9 and 84 +/- 4.7 g/day for the RMG (n=16) and NMG (n=10) groups respectively, and body condition score immediately prior to parturition was higher in RMG than in NMG ewes (2.9 +/- 0.04 vs 1.9 +/- 0.15 score units respectively, P<0.001). For the RMG and NMG groups respectively, mean placental weight was 327 +/- 18.1 and 485 +/- 16.6 g with lamb birth weights of 3.49 +/- 0.13 and 4.82 +/- 0.21 kg (P<0.001). The reduction in placental mass in the RMG group reflected a decrease in the number (P<0.001) and size (P<0.01) of the fetal cotyledons. The duration of gestation was shorter (P<0.001) and colostrum yield at parturition lower (P<0.001) in the RMG group. Maternal insulin concentrations, determined three times weekly, were higher (P<0.001) throughout gestation in the RMG group and irrespective of treatment group were negatively correlated (P<0.01) with placental weight and lamb birth weight. High glucose levels throughout gestation and a decreased response to an exogenous insulin challenge on day 95 of gestation implied a degree of insulin resistance in the RMG group but, in spite of these high maternal glucose concentrations, the reduced size of the placenta probably constrained fetal growth. Maternal IGF-I levels determined weekly, were elevated (P<0.001) during the second and third trimester in RMG versus NMG groups and a sustained elevation in maternal tri-iodothyronine and thyroxine concentrations was evident in the RMG group from mid-gestation. In contrast, GH pulse frequency and mean GH concentrations, determined on day 68 and 122 of gestation, were lower (P<0.05) in the RMG group, and irrespective of treatment group, were correlated negatively with feed intake and positively with placental weight and colostrum yield at parturition. Progesterone concentrations were lower in the RMG group during the second and third trimesters (P<0.001) and, irrespective of treatment group, were positively associated (P<0.001) with placental weight, gestation length and colostrum yield. These results suggest that in pregnant adolescent sheep on high dietary intakes, elevated insulin and IGF-I levels ensure that the anabolic drive to maternal tissue synthesis is established during early gestation at the expense of placental growth.

The consequent restriction in placental transport capacity is the primary limitation to fetal growth and reduced GH and placental progesterone secretion may impair colostrum production.

Original languageEnglish
Pages (from-to)359-368
Number of pages10
JournalJournal of Endocrinology
Volume155
Issue number2
Publication statusPublished - Nov 1997

Keywords

  • GROWTH-FACTOR-I
  • FETAL GROWTH
  • PLACENTAL-LACTOGEN
  • PROTEIN-METABOLISM
  • ADIPOSE-TISSUE
  • MAMMARY-GLAND
  • BINDING-PROTEINS
  • SKELETAL-MUSCLE
  • INSULIN
  • GLUCOSE

Cite this

Maternal endocrine status in relation to pregnancy outcome in rapidly growing adolescent sheep. / Wallace, Jacqueline; DaSilva, P ; Aitken, Raymond; Cruickshank, Morven.

In: Journal of Endocrinology, Vol. 155, No. 2, 11.1997, p. 359-368.

Research output: Contribution to journalArticle

Wallace, Jacqueline ; DaSilva, P ; Aitken, Raymond ; Cruickshank, Morven. / Maternal endocrine status in relation to pregnancy outcome in rapidly growing adolescent sheep. In: Journal of Endocrinology. 1997 ; Vol. 155, No. 2. pp. 359-368.
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T1 - Maternal endocrine status in relation to pregnancy outcome in rapidly growing adolescent sheep

AU - Wallace, Jacqueline

AU - DaSilva, P

AU - Aitken, Raymond

AU - Cruickshank, Morven

PY - 1997/11

Y1 - 1997/11

N2 - It has previously been reported that high nutrient intakes which promote rapid maternal growth throughout pregnancy are associated with poor pregnancy outcome when compared with normally growing adolescent animals. The present study examined the maternal plasma concentrations of a number of putative endocrine regulators of nutrient partitioning between the maternal and fetal compartments in relation to placental and fetal growth in this novel experimental paradigm. Embryos were recovered on day 4 after oestrus fi-om superovulated adult ewes that had been inseminated using semen from a single sire and synchronously transferred, in singleton, to the uterus of peripubertal adolescent recipients (n=38), which had been induced to ovulate at 32 weeks of age Give weight 47.4+/-0.4 kg). Post-transfer, the adolescent recipients were offered a high (n=21) or moderate (n=17) level of a complete diet calculated to achieve rapid (RMG) or normal (NMG) maternal growth rates. After day 100 of gestation, the feed intake of the NMG group was adjusted weekly to meet the increasing nutrient demands of the gravid uterus. Pregnancy rate following embryo transfer was higher (P<0.05) in the RMG (90%) than in the NMG (59%) group. For ewes delivering live young at term, liveweight gain during the first 100 days of gestation was 294 +/- 12.9 and 84 +/- 4.7 g/day for the RMG (n=16) and NMG (n=10) groups respectively, and body condition score immediately prior to parturition was higher in RMG than in NMG ewes (2.9 +/- 0.04 vs 1.9 +/- 0.15 score units respectively, P<0.001). For the RMG and NMG groups respectively, mean placental weight was 327 +/- 18.1 and 485 +/- 16.6 g with lamb birth weights of 3.49 +/- 0.13 and 4.82 +/- 0.21 kg (P<0.001). The reduction in placental mass in the RMG group reflected a decrease in the number (P<0.001) and size (P<0.01) of the fetal cotyledons. The duration of gestation was shorter (P<0.001) and colostrum yield at parturition lower (P<0.001) in the RMG group. Maternal insulin concentrations, determined three times weekly, were higher (P<0.001) throughout gestation in the RMG group and irrespective of treatment group were negatively correlated (P<0.01) with placental weight and lamb birth weight. High glucose levels throughout gestation and a decreased response to an exogenous insulin challenge on day 95 of gestation implied a degree of insulin resistance in the RMG group but, in spite of these high maternal glucose concentrations, the reduced size of the placenta probably constrained fetal growth. Maternal IGF-I levels determined weekly, were elevated (P<0.001) during the second and third trimester in RMG versus NMG groups and a sustained elevation in maternal tri-iodothyronine and thyroxine concentrations was evident in the RMG group from mid-gestation. In contrast, GH pulse frequency and mean GH concentrations, determined on day 68 and 122 of gestation, were lower (P<0.05) in the RMG group, and irrespective of treatment group, were correlated negatively with feed intake and positively with placental weight and colostrum yield at parturition. Progesterone concentrations were lower in the RMG group during the second and third trimesters (P<0.001) and, irrespective of treatment group, were positively associated (P<0.001) with placental weight, gestation length and colostrum yield. These results suggest that in pregnant adolescent sheep on high dietary intakes, elevated insulin and IGF-I levels ensure that the anabolic drive to maternal tissue synthesis is established during early gestation at the expense of placental growth.The consequent restriction in placental transport capacity is the primary limitation to fetal growth and reduced GH and placental progesterone secretion may impair colostrum production.

AB - It has previously been reported that high nutrient intakes which promote rapid maternal growth throughout pregnancy are associated with poor pregnancy outcome when compared with normally growing adolescent animals. The present study examined the maternal plasma concentrations of a number of putative endocrine regulators of nutrient partitioning between the maternal and fetal compartments in relation to placental and fetal growth in this novel experimental paradigm. Embryos were recovered on day 4 after oestrus fi-om superovulated adult ewes that had been inseminated using semen from a single sire and synchronously transferred, in singleton, to the uterus of peripubertal adolescent recipients (n=38), which had been induced to ovulate at 32 weeks of age Give weight 47.4+/-0.4 kg). Post-transfer, the adolescent recipients were offered a high (n=21) or moderate (n=17) level of a complete diet calculated to achieve rapid (RMG) or normal (NMG) maternal growth rates. After day 100 of gestation, the feed intake of the NMG group was adjusted weekly to meet the increasing nutrient demands of the gravid uterus. Pregnancy rate following embryo transfer was higher (P<0.05) in the RMG (90%) than in the NMG (59%) group. For ewes delivering live young at term, liveweight gain during the first 100 days of gestation was 294 +/- 12.9 and 84 +/- 4.7 g/day for the RMG (n=16) and NMG (n=10) groups respectively, and body condition score immediately prior to parturition was higher in RMG than in NMG ewes (2.9 +/- 0.04 vs 1.9 +/- 0.15 score units respectively, P<0.001). For the RMG and NMG groups respectively, mean placental weight was 327 +/- 18.1 and 485 +/- 16.6 g with lamb birth weights of 3.49 +/- 0.13 and 4.82 +/- 0.21 kg (P<0.001). The reduction in placental mass in the RMG group reflected a decrease in the number (P<0.001) and size (P<0.01) of the fetal cotyledons. The duration of gestation was shorter (P<0.001) and colostrum yield at parturition lower (P<0.001) in the RMG group. Maternal insulin concentrations, determined three times weekly, were higher (P<0.001) throughout gestation in the RMG group and irrespective of treatment group were negatively correlated (P<0.01) with placental weight and lamb birth weight. High glucose levels throughout gestation and a decreased response to an exogenous insulin challenge on day 95 of gestation implied a degree of insulin resistance in the RMG group but, in spite of these high maternal glucose concentrations, the reduced size of the placenta probably constrained fetal growth. Maternal IGF-I levels determined weekly, were elevated (P<0.001) during the second and third trimester in RMG versus NMG groups and a sustained elevation in maternal tri-iodothyronine and thyroxine concentrations was evident in the RMG group from mid-gestation. In contrast, GH pulse frequency and mean GH concentrations, determined on day 68 and 122 of gestation, were lower (P<0.05) in the RMG group, and irrespective of treatment group, were correlated negatively with feed intake and positively with placental weight and colostrum yield at parturition. Progesterone concentrations were lower in the RMG group during the second and third trimesters (P<0.001) and, irrespective of treatment group, were positively associated (P<0.001) with placental weight, gestation length and colostrum yield. These results suggest that in pregnant adolescent sheep on high dietary intakes, elevated insulin and IGF-I levels ensure that the anabolic drive to maternal tissue synthesis is established during early gestation at the expense of placental growth.The consequent restriction in placental transport capacity is the primary limitation to fetal growth and reduced GH and placental progesterone secretion may impair colostrum production.

KW - GROWTH-FACTOR-I

KW - FETAL GROWTH

KW - PLACENTAL-LACTOGEN

KW - PROTEIN-METABOLISM

KW - ADIPOSE-TISSUE

KW - MAMMARY-GLAND

KW - BINDING-PROTEINS

KW - SKELETAL-MUSCLE

KW - INSULIN

KW - GLUCOSE

M3 - Article

VL - 155

SP - 359

EP - 368

JO - Journal of Endocrinology

JF - Journal of Endocrinology

SN - 0022-0795

IS - 2

ER -