Effect of Variable Long-Term Maternal Feed Allowance on the Development of the Ovine Placenta and Fetus
Introduction
Perturbations of the pre-natal environment can affect the development of the fetus and placenta, subsequently impacting on post-natal viability and productivity. These latter aspects have implications for the fields of agriculture and medicine.
The effects of intrauterine growth retardation (IUGR) via artificial methods (e.g. carunclectomy) [1], maternal under-nutrition [2], [3], maternal nutrient partitioning (e.g. adolescent ewe model) [4], [5] and litter size (e.g. prolific ewe model) [6] on ovine fetal development are widely reported. Severe restrictions of substrate supply may result in maternal, placental and fetal adaptations to the altered pre-natal environment, which allows survival of offspring, often at the expense of normal fetal development. There is increasing evidence from epidemiological and experimental studies that the programming of fetal development may be particularly sensitive to maternal nutrient status during the peri-conception period. Changes in maternal live weight [7] and differences in ewe body condition score [8] prior to mating have been related to altered utero-placental weights at days 53–56 and 65 of gestation, respectively, in sheep. However, no studies appear to have investigated if these differences persist throughout pregnancy.
Perturbed fetal development may be apparent as altered fetal/birth weight, length, girth and disproportionate tissue growth. There is a tendency for substrates to be directed to maintain essential tissues and organs, such as the brain, at the expense of less vital ones. As a result, size at birth, muscle development and growth [9], [10], wool follicle formation [11], adiposity [6], [12] and gastrointestinal tract development [13] may be altered in growth restricted fetuses and newborns. Such perturbations in development may affect neonatal survival or influence post-natal productivity of livestock.
Adaptations of the fetus to restricted nutrient supply not only alter post-natal performance but are also considered likely precursors to adulthood disease in humans. These fetal adaptations are often associated with fetal hypoglycaemia, hypoxaemia and modifications to the insulin-like growth factor (IGF) and hypothalmo-pituitary-adrenal axes. A number of epidemiology studies have implicated these fetal adaptations to placental insufficiency with diseases later in life [14].
The following experiment examined the hypothesis that long-term pre- and post-conception feed allowance of the ewe induces adaptations in feto-placental and maternal characteristics and affects the development of the ovine fetus. Some of the mechanisms responsible for these adaptations were investigated.
Section snippets
Materials and methods
The experimental protocol was reviewed and approved by the Primary Industries and Resources South Australia, Animal Ethics Committee in accordance with the Australian Code of Practice for the Care and Use of Animals for Scientific Purposes [15].
Maternal live weight and condition score
Live weights and condition scores of R and AL ewes differed significantly from 50 days prior to insemination, at insemination and on allocated days of slaughter (P < 0.05, Table 1). Ewe live weight increased significantly between days 92 and 133 of pregnancy (P < 0.05) in all treatment groups, even though feed allowances remained fixed at initial treatment levels and condition scores of treatment groups continued to diverge. Nevertheless, AL ewes were 30–40% heavier than their R counterparts at late
Discussion
The present study is unique in the timing of onset and duration of the maternal feed restriction imposed. It is the only study in which fetal, placental and maternal characteristics were quantified at three stages of gestation in ewes that were already significantly divergent in live weight and body condition score from approximately 50 days prior to conception as well as throughout gestation.
Differential maternal feed allowance coupled with variable litter size, resulted in compensatory
Acknowledgements
The assistance of Karen Kind, Kathy Gatford and Melissa Bradbury (Research Centre for Research Centre for Early Origins of Adult Disease, University of Adelaide) and the Turretfield Farm staff in fetal and placental collections is gratefully acknowledged. Simon Humphrys (Primegro LTD) conducted the IGF assays on fetal plasma samples. This work was supported by SARDI Livestock Systems.
References (44)
- et al.
Effects of long term undernutrition of the ewe on the growth rates of individual fetuses during late pregnancy
Res Vet Sci
(1982) - et al.
Relationship between nutritionally-mediated placental growth restriction and fetal growth, body composition and endocrine status during late gestation in adolescent sheep
Placenta
(2000) - et al.
Restriction of nutrition in utero selectively inhibits gastro intestinal growth in fetal sheep
J Nutr
(1997) - et al.
The effects of acute nutrient restriction in the mid-gestational ewe on maternal and fetal nutrient status, the expression of placental growth factors and fetal growth
Placenta
(2005) - et al.
Mice carrying null mutations of the genes encoding insulin-like growth factor 1 (IGF-I) and type I IGF receptor (IGFIr)
Cell
(1993) - et al.
Experimental fetal growth retardation: metabolic and endocrine aspects. Research in perinatal medicine (VIII). Advances in fetal physiology: reviews in honour of G.C
Liggins
(1989) Factors affecting foetal growth and development of Merino sheep with particular reference to maternal nutrition
Faculty of Agricultural Science
(1965)- et al.
Nutrient partitioning during adolescent pregnancy
Reproduction
(2001) - et al.
Effects of birth weight and postnatal nutrition on neonatal sheep: I. Body growth and composition and some aspects of energetic efficiency
J Anim Sci
(1998) - et al.
Periconceptional nutrition and the relationship between maternal body weight changes in the periconceptional period and feto-placental growth in the sheep
J Physiol
(2005)
Effect of maternal body condition on placental and fetal growth and the insulin-like growth factor axis in Dorset ewes
Reproduction
Intrauterine growth retardation is associated with reduced cell cycle activity, but not myofibre number, in ovine fetal muscle
Reprod Fert Dev
Effects of birth weight and postnatal nutrition on neonatal sheep: II. Skeletal muscle growth and development
J Anim Sci
The influence of nutritional level during pre-natal and early post-natal life on adult fleece and body characters
Aust J Agric Res
Nutritional manipulation of fetal adipose tissue deposition and uncoupling protein 1 messenger RNA abundance in the sheep: differential effects of timing and duration
Biol Reprod
Mothers, babies and health in later life
Australian code of practice for the care and use of animals for scientific purposes
Energy and protein requirements of ruminants
Subjective assessment of body fat in live sheep
J Agric Sci (Camb)
Growth and metabolism of the placenta after unilateral fetectomy in twin pregnant ewes
J Dev Physiol
Growth hormone increases insulin-like growth factor-I (IGF-I) and decreases IGF-II in plasma of growing pigs
J Endocrinol
The GLM procedure
SAS Procedures Guide
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Effect of prepartum maternal energy density on the growth performance, immunity, and antioxidation capability of neonatal calves
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