Effects of High-Fat Diet at Two Energetic Levels on Fecal Microbiota, Colonic Barrier, and Metabolic Parameters in Dogs

Increased consumption of energy-rich foods is a key factor in overweight, obesity, and associated metabolic disorders. This would be, at least in part, related to microbiota disturbance. In rodent models of obesity, microbiota disruption has been associated with alteration of the intestinal barrier,...

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Main Authors: Alex Moinard, Cyrielle Payen, Khadija Ouguerram, Agnès André, Juan Hernandez, Amandine Drut, Vincent C. Biourge, Jan S. Suchodolski, John Flanagan, Patrick Nguyen, Véronique Leray
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-09-01
Series:Frontiers in Veterinary Science
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Online Access:https://www.frontiersin.org/article/10.3389/fvets.2020.566282/full
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author Alex Moinard
Cyrielle Payen
Khadija Ouguerram
Agnès André
Juan Hernandez
Amandine Drut
Vincent C. Biourge
Jan S. Suchodolski
John Flanagan
Patrick Nguyen
Véronique Leray
author_facet Alex Moinard
Cyrielle Payen
Khadija Ouguerram
Agnès André
Juan Hernandez
Amandine Drut
Vincent C. Biourge
Jan S. Suchodolski
John Flanagan
Patrick Nguyen
Véronique Leray
author_sort Alex Moinard
collection DOAJ
description Increased consumption of energy-rich foods is a key factor in overweight, obesity, and associated metabolic disorders. This would be, at least in part, related to microbiota disturbance. In rodent models of obesity, microbiota disruption has been associated with alteration of the intestinal barrier, endotoxemia, inflammation grade, and insulin sensitivity. The aim of the present study was to assess the effects of a high-fat diet (HFD), fed at two energetic levels, on microbiota, intestinal barrier, and inflammatory and metabolic parameters in dogs. A HFD (33% fat as fed, 4,830 kcal/kg) was given to 24 healthy Beagle dogs at 100% (HF-100; n = 8) and at 150% (HF-150; n = 16) of their maintenance energy requirements for 8 weeks. Analysis of similarity revealed a significant difference in gut microbiota β-diversity following the diet compared to week 0 in both groups while α-diversity was lower only in the HF-150 group. Firmicutes/Bacteroidetes ratio was higher in the HF-150 group compared to the HF-100 group at weeks 2 and 8. A reduction in insulin sensitivity was observed over time in the HF150 group. Neither endotoxemia nor inflammation was observed in either group, did not find supporting data for the hypothesis that the microbiota is involved in the decline of insulin sensitivity through metabolic endotoxemia and low-grade inflammation. Colonic permeability was increased at week 4 in both groups and returned to initial levels at week 8, and was associated with modifications to the expression of genes involved in colonic barrier function. The increase in intestinal permeability may have been caused by the altered intestinal microbiota and increased expression of genes encoding tight junction proteins might indicate a compensatory mechanism to restore normal permeability. Although simultaneous changes to the microbiota, barrier permeability, inflammatory, and metabolic status have not been observed, such a causal link cannot be excluded in dogs overfed on a HFD. Further studies are necessary to better understand the link between HFD, intestinal microbiota and the host.
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spelling doaj.art-8f22c7b00ad746f4a7e9975ca90e76ce2022-12-22T01:22:44ZengFrontiers Media S.A.Frontiers in Veterinary Science2297-17692020-09-01710.3389/fvets.2020.566282566282Effects of High-Fat Diet at Two Energetic Levels on Fecal Microbiota, Colonic Barrier, and Metabolic Parameters in DogsAlex Moinard0Cyrielle Payen1Khadija Ouguerram2Agnès André3Juan Hernandez4Amandine Drut5Vincent C. Biourge6Jan S. Suchodolski7John Flanagan8Patrick Nguyen9Véronique Leray10Nutrition, PhysioPathology and Pharmacology Unit (NP3), Oniris, College of Veterinary Medicine, Food Sciences and Engineering, CRNH, Nantes, FranceNutrition, PhysioPathology and Pharmacology Unit (NP3), Oniris, College of Veterinary Medicine, Food Sciences and Engineering, CRNH, Nantes, FranceUMR 1280 Physiopathology of Nutritional Adaptations (PhAN), INRAE, CRNH, West Human Nutrition Research Center, CHU, Nantes, FranceNutrition, PhysioPathology and Pharmacology Unit (NP3), Oniris, College of Veterinary Medicine, Food Sciences and Engineering, CRNH, Nantes, FranceUSC 1383 Cellular and Molecular Immunoendocrinology (IECM), INRAE, Oniris, College of Veterinary Medicine, Food Sciences and Engineering, Nantes, FranceNutrition, PhysioPathology and Pharmacology Unit (NP3), Oniris, College of Veterinary Medicine, Food Sciences and Engineering, CRNH, Nantes, FranceResearch Center, Royal Canin SAS, Aimargues, FranceGastrointestinal Laboratory, Texas A&M University, College Station, TX, United StatesResearch Center, Royal Canin SAS, Aimargues, FranceNutrition, PhysioPathology and Pharmacology Unit (NP3), Oniris, College of Veterinary Medicine, Food Sciences and Engineering, CRNH, Nantes, FranceNutrition, PhysioPathology and Pharmacology Unit (NP3), Oniris, College of Veterinary Medicine, Food Sciences and Engineering, CRNH, Nantes, FranceIncreased consumption of energy-rich foods is a key factor in overweight, obesity, and associated metabolic disorders. This would be, at least in part, related to microbiota disturbance. In rodent models of obesity, microbiota disruption has been associated with alteration of the intestinal barrier, endotoxemia, inflammation grade, and insulin sensitivity. The aim of the present study was to assess the effects of a high-fat diet (HFD), fed at two energetic levels, on microbiota, intestinal barrier, and inflammatory and metabolic parameters in dogs. A HFD (33% fat as fed, 4,830 kcal/kg) was given to 24 healthy Beagle dogs at 100% (HF-100; n = 8) and at 150% (HF-150; n = 16) of their maintenance energy requirements for 8 weeks. Analysis of similarity revealed a significant difference in gut microbiota β-diversity following the diet compared to week 0 in both groups while α-diversity was lower only in the HF-150 group. Firmicutes/Bacteroidetes ratio was higher in the HF-150 group compared to the HF-100 group at weeks 2 and 8. A reduction in insulin sensitivity was observed over time in the HF150 group. Neither endotoxemia nor inflammation was observed in either group, did not find supporting data for the hypothesis that the microbiota is involved in the decline of insulin sensitivity through metabolic endotoxemia and low-grade inflammation. Colonic permeability was increased at week 4 in both groups and returned to initial levels at week 8, and was associated with modifications to the expression of genes involved in colonic barrier function. The increase in intestinal permeability may have been caused by the altered intestinal microbiota and increased expression of genes encoding tight junction proteins might indicate a compensatory mechanism to restore normal permeability. Although simultaneous changes to the microbiota, barrier permeability, inflammatory, and metabolic status have not been observed, such a causal link cannot be excluded in dogs overfed on a HFD. Further studies are necessary to better understand the link between HFD, intestinal microbiota and the host.https://www.frontiersin.org/article/10.3389/fvets.2020.566282/fullhigh-fat diet (HFD)microbiota (microorganism)colonic barrierinsulin sensitivitydog
spellingShingle Alex Moinard
Cyrielle Payen
Khadija Ouguerram
Agnès André
Juan Hernandez
Amandine Drut
Vincent C. Biourge
Jan S. Suchodolski
John Flanagan
Patrick Nguyen
Véronique Leray
Effects of High-Fat Diet at Two Energetic Levels on Fecal Microbiota, Colonic Barrier, and Metabolic Parameters in Dogs
Frontiers in Veterinary Science
high-fat diet (HFD)
microbiota (microorganism)
colonic barrier
insulin sensitivity
dog
title Effects of High-Fat Diet at Two Energetic Levels on Fecal Microbiota, Colonic Barrier, and Metabolic Parameters in Dogs
title_full Effects of High-Fat Diet at Two Energetic Levels on Fecal Microbiota, Colonic Barrier, and Metabolic Parameters in Dogs
title_fullStr Effects of High-Fat Diet at Two Energetic Levels on Fecal Microbiota, Colonic Barrier, and Metabolic Parameters in Dogs
title_full_unstemmed Effects of High-Fat Diet at Two Energetic Levels on Fecal Microbiota, Colonic Barrier, and Metabolic Parameters in Dogs
title_short Effects of High-Fat Diet at Two Energetic Levels on Fecal Microbiota, Colonic Barrier, and Metabolic Parameters in Dogs
title_sort effects of high fat diet at two energetic levels on fecal microbiota colonic barrier and metabolic parameters in dogs
topic high-fat diet (HFD)
microbiota (microorganism)
colonic barrier
insulin sensitivity
dog
url https://www.frontiersin.org/article/10.3389/fvets.2020.566282/full
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