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Feeding non-ruminants a high-fat high-fiber diet: differences in adaptive responses between growing pigs and chickens

In pigs, body adiposity was reduced by the distribution of a high-fat high-fiber diet when compared to a high-starch diet. This was associated to the reduction in expression levels of many genes regulating glucose and lipid metabolisms in adipose tissues; possible effects of this diet on immunity and inflammation were also suggested. In chickens, feeding a high-fat high-fiber diet did not affect growth and body composition and the hepatic metabolism played a key role in this adaptation.

Aliment porc riche en lipides (80g/kg) et fibres et aliment pauvre en lipides (20g/kg) et fibres. © INRA, .
Updated on 08/22/2016
Published on 07/13/2016

Context and challenge:

Body fatness and fat distribution in the body are important concerns in animal production because these traits contribute to the efficiency of meat production and robustness of animals. Lipid metabolic flexibility, which is responsible for the storage and use of lipids within the body, can be considered to improve animal adaptation to different regimen. The competition between food and feed challenges the use of alternative resources such as fibrous feedstuffs in diets formulated for non-ruminants, whereas adding fat to a high-fiber diet appears as a relevant strategy to improve its dietary energy value; however, this changes nutrients and energy source compared to a standard cereal-based high-starch diet. A better understanding of the metabolic ways by which growing animals may adapt to high-fat high-fiber diets is essential to refine nutritional recommendations and suggest adiposity biomarkers that can be used in precision farming and next selection schemes.

Results:

Various physiological and phenotypic data and thousand molecular data in different tissues were acquired in growing animals fed iso-caloric and iso-proteic diets but different in nutrient composition and energy source (fibers and lipids vs. starch). Growth performance and body adiposity were reduced in pigs fed a diet rich in fat and fiber (mainly insoluble) when compared with pigs fed a standard high-starch diet. The main biological pathways involved in these changes were related to glucose and lipid metabolisms, protein catabolism process, apoptosis, modulation of oxidative stress and immune or inflammatory defense mechanisms. Key upstream regulators in these pathways were proposed, such as MLXIPL, SREBF1, PPARD and RXRA genes; these transcription factors must be considered in next programs aiming to manage body composition. Unlike pigs, feeding chicken a high-fat high-fiber diet did not affect growth performance and body composition: irrespective of dietary differences in fat content and energy source, chickens can synthesize the same amount of fat in tissues. The hepatic metabolism played a key role in this adaptation, with a decrease in lipogenesis and glycogen synthesis but an increase in oxidative pathways. We also observed that a massive duplication of free fatty acids receptors (FFAR2) that are activated by short-chain free fatty acids produced by the intestinal digestion of soluble fibers, occurred in the chicken genome along evolution. In both species, biomarkers of body adiposity were also identified in the blood, such as CPT1A gene whose expression was increased by a high-fat high-fiber diet.

Perspectives:

This study emphasizes the benefits of nutrigenomics to identify key actors in cellular flexibility and tissue adaptation. The variety in the metabolic responses to diets shows that it is important to consider traits related to productive functions but also to non-productive functions (immunity, inflammation or oxidative stress) for the nutritional recommendations in poultry and pigs. The comparison between species generates new questions about adaptive strategies and animal robustness.

References

Gondret F, Louveau I, Mourot J, Duclos MJ, Lagarrigue S, Gilbert H, van Milgen J. Dietary energy sources affect the partition of body lipids and the hierarchy of energy metabolic pathways in growing pigs differing in feed efficiency. J. Anim. Sci. 2014; 92: 4865-77.

Baéza E, Gondret F, Chartrin P, Le Bihan-Duval E, Berri C, Gabriel I, Narcy A, Lessire M, Métayer-Coustard S, Collin A, Jégou M, Lagarrigue S, Duclos MJ. The ability of genetically lean or fat slow-growing chickens to synthesize and store lipids is not altered by the dietary energy source. Animal. 2015; 9: 1643-52.

Jégou M, Gondret F, Lalande-Martin J, Tea I, Baéza E, Louveau I. NMR-based metabolomics highlights differences in plasma metabolites in pigs exhibiting diet-induced differences in adiposity. Eur. J. Nutr. 2015 May 22.

Meslin C, Desert C, Callebaut I, Djari A, Klopp C, Pitel F, Leroux S, Martin P, Froment P, Guilbert E, Gondret F, Lagarrigue S, Monget P. Genome Biol. Evol. 2015; 7: 1332-48.

Baéza E, Jégou M, Gondret F, Lalande-Martin J, Tea I, Le Bihan-Duval E, Berri C, Collin A, Métayer-Coustard S, Louveau I, Lagarrigue S, Duclos MJ. Pertinent plasma indicators of the ability of chickens to synthesize and store lipids. J. Anim. Sci. 2015; 93: 107-116

Publication/patent

This work was carried out by INRA Units Pegase, URA and PRC and in collaboration with IRISA and Agrocampus-Ouest; it was granted by ANR (FatInteger project SVSE7-04-11). This was also part of the PhD of Maëva Jégou, funded by INRA (Phase division) and Région Bretagne.