High-fat diet reduces the formation of butyrate, but increases succinate, inflammation, liver fat and cholesterol in rats, while dietary fibre counteracts these effects

PLoS One. 2013 Nov 13;8(11):e80476. doi: 10.1371/journal.pone.0080476. eCollection 2013.

Abstract

Introduction: Obesity is linked to type 2 diabetes and risk factors associated to the metabolic syndrome. Consumption of dietary fibres has been shown to have positive metabolic health effects, such as by increasing satiety, lowering blood glucose and cholesterol levels. These effects may be associated with short-chain fatty acids (SCFAs), particularly propionic and butyric acids, formed by microbial degradation of dietary fibres in colon, and by their capacity to reduce low-grade inflammation.

Objective: To investigate whether dietary fibres, giving rise to different SCFAs, would affect metabolic risk markers in low-fat and high-fat diets using a model with conventional rats for 2, 4 and 6 weeks.

Material and methods: Conventional rats were administered low-fat or high-fat diets, for 2, 4 or 6 weeks, supplemented with fermentable dietary fibres, giving rise to different SCFA patterns (pectin - acetic acid; guar gum - propionic acid; or a mixture - butyric acid). At the end of each experimental period, liver fat, cholesterol and triglycerides, serum and caecal SCFAs, plasma cholesterol, and inflammatory cytokines were analysed. The caecal microbiota was analysed after 6 weeks.

Results and discussion: Fermentable dietary fibre decreased weight gain, liver fat, cholesterol and triglyceride content, and changed the formation of SCFAs. The high-fat diet primarily reduced formation of SCFAs but, after a longer experimental period, the formation of propionic and acetic acids recovered. The concentration of succinic acid in the rats increased in high-fat diets with time, indicating harmful effect of high-fat consumption. The dietary fibre partly counteracted these harmful effects and reduced inflammation. Furthermore, the number of Bacteroides was higher with guar gum, while noticeably that of Akkermansia was highest with the fibre-free diet.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Body Weight
  • Butyrates / blood
  • Butyrates / metabolism*
  • Chemokine CCL2 / blood
  • Cholesterol / blood
  • Cholesterol / metabolism*
  • Colon / metabolism
  • Colon / microbiology
  • Diet
  • Diet, High-Fat / adverse effects*
  • Dietary Fiber / metabolism*
  • Fatty Acids, Volatile / blood
  • Fatty Acids, Volatile / metabolism
  • Inflammation / metabolism*
  • Liver / metabolism*
  • Liver / pathology*
  • Male
  • Microbiota
  • Organ Size
  • Pectins / metabolism
  • Rats
  • Succinic Acid / blood
  • Succinic Acid / metabolism*
  • Time Factors

Substances

  • Butyrates
  • Chemokine CCL2
  • Dietary Fiber
  • Fatty Acids, Volatile
  • Pectins
  • Cholesterol
  • Succinic Acid

Grant support

This study was supported by the Antidiabetic Food Centre, a VINNOVA VINN Excellence Center at Lund University (http://www.ffsc.lu.se/afc), and Sparbanksstiftelsen Färs & Frosta and Skåneländska Gastronomiska Akademien. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.