Impacts of prenatal nutrition on animal production and performance: a focus on growth and metabolic and endocrine function in sheep

Abstract

The concept of foetal programming (FP) originated from human epidemiological studies, where foetal life nutrition was linked to health and disease status later in life. Since the proposal of this phenomenon, it has been evaluated in various animal models to gain further insights into the mechanisms underlying the foetal origins of health and disease in humans. In FP research, the sheep has been quite extensively used as a model for humans. In this paper we will review findings mainly from our Copenhagen sheep model, on the implications of late gestation malnutrition for growth, development, and metabolic and endocrine functions later in life, and discuss how these implications may depend on the diet fed to the animal in early postnatal life. Our results have indicated that negative implications of foetal malnutrition, both as a result of overnutrition and, particularly, late gestation undernutrition, can impair a wide range of endocrine functions regulating growth and presumably also reproductive traits. These implications are not readily observable early in postnatal life, but are increasingly manifested as the animal approaches adulthood. No intervention or cure is known that can reverse this programming in postnatal life. Our findings suggest that close to normal growth and slaughter results can be obtained at least until puberty in animals which have undergone adverse programming in foetal life, but manifestation of programming effects becomes increasingly evident in adult animals. Due to the risk of transfer of the adverse programming effects to future generations, it is therefore recommended that animals that are suspected to have undergone adverse FP are not used for reproduction. Unfortunately, no reliable biomarkers have as yet been identified that allow accurate identification of adversely programmed offspring at birth, except for very low or high birth weights, and, in pigs, characteristic changes in head shape (dolphin head). Future efforts should be therefore dedicated to identify reliable biomarkers and evaluate their effectiveness for alleviation/reversal of the adverse programming in postnatal life. Our sheep studies have shown that the adverse impacts of an extreme, high-fat diet in early postnatal life, but not prenatal undernutrition, can be largely reversed by dietary correction later in life. Thus, birth (at term) appears to be a critical set point for permanent programming in animals born precocial, such as sheep. Appropriate attention to the nutrition of the late pregnant dam should therefore be a priority in animal production systems.

Gestation Food Restriction and Refeeding Compensate Maternal Energy Status and Alleviate Metabolic Consequences in Juvenile Offspring in a Rabbit Model

“…This adaptation called "fetal programming" is beneficial for survival under undernourishment in the uterus, but detrimental when nutrition is abundant in post-natal life [9]. It highly depends on the timing of disturb takes place (i.e., embryogenesis, organogenesis, or organ growth) [10,11], and on the severity of the insult [12,13].…”

Effects of Birth Weight on Animal Performance, Fattening Traits and Meat Quality of Lambs

“…Aligned with this statement, it must be mentioned that increased adiposity after a fattening period of early feed-restricted lambs (postnatal) is partially a consequence of insulin resistance patterns developed during early life, which may affect meat quality traits (e.g., more saturated intramuscular fat) [ 8 ]. These long-term effects of maternal nutrition (e.g., higher body fat deposition, low formation of lean muscle, obesity and metabolic syndrome) can be embraced under concepts such as the thrifty phenotype hypothesis, fetal programming (pre-natal feed restriction in utero) or developmental origins of health and disease (DOHaD, describing both pre- and post-natal feed restriction) [ 9 , 10 , 11 , 12 ]. Understanding how low body birth weight affects all these traits (body composition, carcass characteristics, organ development and meat quality (e.g., texture, fat deposition or fatty acid profile)) might help us to comprehend the reasons behind the high heterogeneity of fattened lambs in Mediterranean countries.…”

Multi-Omic Biogeography of the Gastrointestinal Microbiota of a Pre-Weaned Lamb

“…Early solid feed intake seems to favor microbial colonization and early functional establishment of the different GITs [ 8 , 9 , 10 ]. In addition, glucose and lipid metabolism (especially insulin secretion, adipose tissue sensitivity to insulin and uptake of glucose) in mature sheep are highly affected by diet and nutritional status experienced in prenatal and postnatal phases, as reviewed by Khanal et al [ 11 ], suggesting that functional changes in these phases are fundamental to permanent metabolic programming and nutrient partitioning.…”