A maternal Western diet during gestation and lactation modifies offspring's microbiota activity, blood lipid levels, cognitive responses, and hippocampal neurogenesis in Yucatan pigs.
A suboptimal early nutritional environment (i.e.,excess of energy, sugar, and fat intake) can increase susceptibility to diseases and neurocognitive disorders. The purpose of this study was to investigate in nonobese Yucatan minipigs (Sus scrofa) the impact of maternal diet [standard diet (SD)vs.Western diet (WD)] during gestation and 25 d of lactation on milk composition, blood metabolism, and microbiota activity of sows (n =17) and their piglets (n =65), and on spatial cognition (n =51), hippocampal plasticity (n =17), and food preferences/motivation (n =51) in the progeny. Milk dry matter and lipid content, as well as plasma total cholesterol and free fatty acid (FFA) concentrations (P< 0.05) were higher in WD than in SD sows. Microbiota activity decreased in both WD sows and 100-d-old piglets (P< 0.05 orP< 0.10, depending on short-chain FAs [SCFAs]). At weaning [postnatal day (PND) 25], WD piglets had increased blood triglyceride and FFA levels (P< 0.01). Both SD and WD piglets consumed more of a known SD than an unknown high-fat and -sucrose (HFS) diet (P< 0.0001), but were quicker to obtain HFS rewards compared with SD rewards (P< 0.01). WD piglets had higher working memory (P= 0.015) and reference memory (P< 0.001) scores, which may reflect better cognitive abilities in the task context and a higher motivation for the food rewards. WD piglets had a smaller hippocampal granular cell layer (P= 0.03) and decreased neurogenesis (P< 0.005), but increased cell proliferation (P< 0.001). A maternal WD during gestation and lactation, even in the absence of obesity, has significant consequences for piglets' blood lipid levels, microbiota activity, gut-brain axis, and neurocognitive abilities after weaning.-Val-Laillet, D., Besson, M., Guérin, S., Coquery, N., Randuineau, G., Kanzari, A., Quesnel, H., Bonhomme, N., Bolhuis, J. E., Kemp, B., Blat, S., Le Huërou-Luron, I., Clouard, C. A maternal Western diet during gestation and lactation modifies offspring's microbiota activity, blood lipid levels, cognitive responses, and hippocampal neurogenesis in Yucatan pigs.
Institut National de la Recherche Agronomique (INRA), Unité de Recherche 1341, Alimentation et Adaptations Digestives, Nerveuses et Comportementales (ADNC), St-Gilles, France; david.val-laillet@inra.fr.
David
D
Val-Laillet
Institut National de la Recherche Agronomique (INRA), Unité de Recherche 1341, Alimentation et Adaptations Digestives, Nerveuses et Comportementales (ADNC), St-Gilles, France.
Marie
M
Besson
Institut National de la Recherche Agronomique (INRA), Unité de Recherche 1341, Alimentation et Adaptations Digestives, Nerveuses et Comportementales (ADNC), St-Gilles, France.
Sylvie
S
Guérin
Institut National de la Recherche Agronomique (INRA), Unité de Recherche 1341, Alimentation et Adaptations Digestives, Nerveuses et Comportementales (ADNC), St-Gilles, France.
Nicolas
N
Coquery
Institut National de la Recherche Agronomique (INRA), Unité de Recherche 1341, Alimentation et Adaptations Digestives, Nerveuses et Comportementales (ADNC), St-Gilles, France.
Gwénaëlle
G
Randuineau
Institut National de la Recherche Agronomique (INRA), Unité de Recherche 1341, Alimentation et Adaptations Digestives, Nerveuses et Comportementales (ADNC), St-Gilles, France.
Ameni
A
Kanzari
INRA, Unité Mixte de Recherche (UMR) 1348, Physiologie Environnement et Génétique pour l'Animal et les Systèmes d'Élevage (PEGASE), St-Gilles, France.|Agrocampus Ouest, UMR 1348 PEGASE, Rennes, France; and.
Hélène
H
Quesnel
INRA, Unité Mixte de Recherche (UMR) 1348, Physiologie Environnement et Génétique pour l'Animal et les Systèmes d'Élevage (PEGASE), St-Gilles, France.|Agrocampus Ouest, UMR 1348 PEGASE, Rennes, France; and.
Nathalie
N
Bonhomme
Adaptation Physiology Group, Department of Animal Sciences, Wageningen University Research, Wageningen, The Netherlands.
J Elizabeth
JE
Bolhuis
Adaptation Physiology Group, Department of Animal Sciences, Wageningen University Research, Wageningen, The Netherlands.
Bas
B
Kemp
Institut National de la Recherche Agronomique (INRA), Unité de Recherche 1341, Alimentation et Adaptations Digestives, Nerveuses et Comportementales (ADNC), St-Gilles, France.
Sophie
S
Blat
Institut National de la Recherche Agronomique (INRA), Unité de Recherche 1341, Alimentation et Adaptations Digestives, Nerveuses et Comportementales (ADNC), St-Gilles, France.
Isabelle
I
Le Huërou-Luron
Adaptation Physiology Group, Department of Animal Sciences, Wageningen University Research, Wageningen, The Netherlands.
Caroline
C
Clouard
D000824:Animal Nutritional Physiological Phenomena / Q000502:physiology; D000818:Animals; D000833:Animals, Suckling; D003071:Cognition / Q000502:physiology*; D066273:Diet, Western; D019587:Dietary Supplements; D005260:Female; D006624:Hippocampus / Q000378:metabolism*; D007774:Lactation / Q000502:physiology*; D008055:Lipids / Q000097:blood*; D039382:Maternal Nutritional Physiological Phenomena / Q000502:physiology; D064307:Microbiota / Q000502:physiology*; D008892:Milk / Q000378:metabolism; D013552:Swine
D008055:Lipids
brain; development; early nutrition; eating behavior; metabolism