Nutritional effects of barley products — Mechanisms of action in the intestinal tract

Abstract

Barley is one of the most important crops in the world. Although it is mainly used as the raw material for the production of beer and animal feed, it has recently attracted interest from nutritionists and consumers, due to its high content of dietary fibre, especially β-glucan, and its relation to various positive health effects. The proposed mechanisms behind the health effects are the formation of short-chain fatty acids (SCFA), especially butyric acid, and the modification of the microbiota in the colon.

The work described in this thesis was focused on how the barley variety, malting, fat content and addition of probiotics to the diet affected the formation of SCFA and the composition of the microbiota in the hindgut of rats. The risk factors associated with low-grade inflammation were also studied, as well as levels of amino acids and cholesterol in the portal plasma. For this purpose, two barley varieties (whole-grain barley SW 49427 and Hadm 12011-06, referred to as SW and Hadm, respectively), high and low in dietary fibre and β-glucan content, respectively, four barley malts (caramelized and coloured malt, 50-malt and 350-malt) with different β-glucan contents and colours, and five probiotic strains (Lactobacillus paracasei 87002, Lactobacillus plantarum HEAL 9 and HEAL 19, Bifidobacterium infantis CURE 21 and Lactobacillus rhamnosus 271) were evaluated. The effect of the different probiotic strains was investigated together with malted barley. A conventional rat model, which has been shown to reflect the results concerning dietary fibre fermentation in humans, was used.

All the barley products generally increased the amount of SCFA in the hindgut and portal vein serum of rats, compared with the control groups. SW induced a higher caecal content of acetic acid and propionic acid in rats than Hadm, and in rats fed high-fat diets a higher caecal content of butyric acid was also seen when incorporated in the diet at the same flour level. However, when whole-grain barleys were consumed at the same dietary fibre level, similar profiles of SCFA were found in the rats. This was most probably due to the rather similar dietary fibre compositions of the diets. The increase in SCFA induced by whole-grain barleys was further enhanced by a high-fat content, apart from butyric acid and minor SCFA (iso-butyric acid, iso-valeric acid and valeric acid), which generally decreased to levels similar to those in rats consuming control diets. The effect was more pronounced when the dietary fibre intake was low. Interestingly, barley malts counteracted those effects. Furthermore, rats fed barley malts had lower caecal amounts of succinic acid, an intermediate acid and precursor of butyric acid, than rats given the two whole-grain barley varieties.

A high-fat diet decreased the abundance of total bacteria and Lactobacillus in the caecum, while whole-grain barleys increased the abundance of Lactobacillus. Furthermore, a high-fat diet increased the population of Akkermansia in rats fed whole-grain barleys. The caecal microbiota composition was different in rats fed whole-grain barley, barley malt and the control diet. Barley malt considerably increased the relative abundance of Roseburia, a butyrate-producer, while that of Akkermansia decreased.

A high-fat diet increased the concentration of lipopolysaccharide-binding protein and amino acids in the portal vein plasma and the mRNA expression of toll-like receptor 4 in the distal colon, and tight junction proteins (zonula occludens-1 and occludin) in the small intestine and distal colon, while barley products not only inhibited the increase in the plasma concentration of lipopolysaccharide-binding protein (whole-grain barleys), amino acids and mRNA expression (barley malts) to some extent, but also decreased the plasma concentration of mono¬cyte chemoattractant protein-1 (whole-grain barleys). However, high amount of advanced glycation end-products in the diet impaired the positive effect of barley malts on small intestinal occludin and portal vein amino acids.

Supplementation of the diet with probiotics had no effect on dietary fibre fermentation or SCFA formation, but increased the portal vein concentration of amino acids, and changed the composition of dominant Lactobacillus strains. A cholesterol-lowering effect was only seen with SW, which contributed to the highest amount of β-glucan in the diet.

In conclusion, barley products increased the caecal formation of SCFA, modulated microbiota composition, reduced low-grade inflammation-associated risk factors and lowered plasma cholesterol. The effects were dependent on variety, malting conditions and fat content of the diet, suggesting that the dietary fibre composition and fat content are of the greatest importance. Furthermore, malting could provide a means of changing the characteristics of dietary fibre in order to optimize the positive health effects of barley.

Abstract (Swedish)

Popular Abstract in English

There is a growing prevalence of disorders associated to the metabolic syndrome globally. To reverse this trend lifestyle changes are required. Among dietary factors, dietary fibre that is associated with several health benefits plays an interesting role. Barley is highly unutilized as human food, and it contains high amounts of dietary fibre. The composition of the barley fibres is quite similar as to those in oats, with high amounts of β-glucan, a fibre component that has been reported to decrease blood cholesterol. The whole-grain barley variety, containing the highest amounts of β-glucan in the present work also reduced the level of cholesterol in the blood. The barley malts (low in β-glucan) had no such effects, suggesting that the β-glucan amount is important for cholesterol-lowering effects of dietary fibres from barley.

The mechanisms behind the physiological effects of dietary fibre are rather unknown, but it is increasingly believed that the action of dietary fibre in the gastrointestinal tract plays a key role. The gastrointestinal tract is more than a passage for food digestion and waste excretion; it is also a barrier that protects our inner environment from microorganisms and harmful substances. Recently, it has been found that toxic components (lipopolysaccharides) from some types of bacteria can enter our circulation causing low-grade inflammation and trigger metabolic disorders. The bacteria in colon are normally living in harmony with human hosts, unless the bacterial composition is disturbed by diet, disease or medical treatment. The bacteria mainly live on dietary fibre and produce short-chain fatty acids (SCFA, mainly acetic acid, propionic acid and butyric acid), which are important nutrients for our intestinal cells and have implications in our metabolism and immune system. Butyric acid is of major importance and the preferred fuel for the intestinal cells, and therefore stimulates mucosal cell proliferation, blood flow and oxygen uptake, resulting in a reduced permeability of the colon and a less influx of toxic substances into the circulation. Propionic acid is another interesting SCFA, traditionally connected with metabolic effects, but during recent years, butyric acid has also been highlighted in this respect. Acetic acid is more associated with negative health effects. Different types of dietary fibre give different amounts and patterns of SCFA and it may be possible to design gut metabolites formed and the microbiota composition by diet to achieve a healthier colonic environment.

In this thesis, various barley products, containing different barley varieties (SW or Hadm) or barley malts with different characteristics were studied. The effect of the fat content in the diet and probiotics added to the diet were also evaluated. SCFA in blood and hindgut, gut microbiota and risk factors associated with low-grade inflammation were evaluated using a rat model.

All barley products studied gave high amounts of SCFA in the colon and portal vein blood, and this could be correlated to the dietary fibre content. An increase in the fat content in the whole-grain diet changed the pattern of SCFA and more acetic and propionic acid was produced, but less butyric acid, especially when the fibre intake was low. As compensation, a “new” acid, succinic acid, appeared. Succinic acid can be formed during antibiotic treatment and also when the fibre intake is low, i.e. at a low bacterial activity in colon. Remarkably, when replacing whole-grain barleys with barley malts, having another fibre composition (arabinoxylan instead of β-glucan), and the amount of butyric acid in the portal vein blood were still high in the high-fat condition and the production of succinic acid was reduced. The addition of probiotics did not have any effects on SCFA neither in colon nor in portal vein blood.

Barley products also affected the population and composition of gut microbiota. Intake of the two whole-grain barley varieties increased the abundance of Bifidobacterium and Lactobacillus and decreased the Bacteroides fragilis group. There was also a decrease in Akkermansia, but only with Hadm. When the fat content increased, the abundance of Lactobacillus decreased, while that of Akkermansia increased. Furthermore, there was a lower abundance of the Clostridium leptum group with Hadm. Barley malt had different effects on microbiota compared with whole grain barley. Thus, the relative abundance of Akkermansia decreased, while that of Roseburia, a well-known butyric acid producer, increased. Interestingly, the amount of butyric acid and succinic acid was correlated with the relative abundance of Roseburia and Akkermansia, respectively. The addition of probiotics changed the composition of lactobacilli.

Barley products decreased risk factors associated with low-grade inflammation, a phenomenon that can initiate obesity and insulin resistance. Intake of barley products resulted in a lower concentration of inflammatory markers (lipopolysaccharide-binding protein and monocyte chemoattractant protein-1) in the blood. This may be due to several mechanisms. First, reshaping of the gut microbiota composition may have led to lower amounts of toxic components in the colon, as reflected by a change in the gene expression of a receptor involved in inflammatory signalling. Second, the migration of toxic components into the circulation may also be reduced, due to a higher nutritional status of the colon. Third, the increased amount of SCFA, preferably butyric acid, in the circulation may counteract low-grade inflammation. Intriguingly, high amounts of advanced glycation end-products, formed in food during heat treatment, impaired the effect of barley products on gut barrier function.

In conclusion, consumption of barley products increased the amount of SCFA, including butyric acid, in the hindgut and portal vein blood of rats and changed the composition of gut microbiota. These alterations may alleviate the risk factors associated with low-grade inflammation and boost health benefits. Furthermore, the amount and composition of dietary fibre were important for the performance of barley products. Higher amounts of fat and advanced glycation end-products attenuated the health benefits. However, by selecting the correct variety or by tailoring the process conditions, functional properties and also health effects can be optimized.

• author: Zhong, Yadong
• supervisor: Margareta Nyman
• opponent: Professor Bach Knudsen, Knud Erik, Department of Animal Science - Molecular nutrition and cell biology, Aarhus University, Denmark
• organization: Food for Health Science Centre, Kemicentrum; Department of Food Technology, Engineering and Nutrition
• publishing date: 2015
• type: Thesis
• publication status: published
• subject: Engineering and Technology
• keywords: dietary fibre, malting, probiotics, high-fat diets, short-chain fatty acids, gut microbiota, low-grade inflammation, gene expression, Barley
• pages: 106 pages
• defense location: Lecture hall F, Kemicentrum, Getingevägen 60, Lund University, Faculty of Engineering LTH, Lund
• defense date: 2015-06-15 09:15:00
• ISBN: 978-91-7422-402-3
• project: ANTIDIABETIC FOOD CENTRE
• language: English
• LU publication?: yes
• id: 56e199b3-5354-49ac-8f86-8d66df5269c1 (old id 5421766)
• date added to LUP: 2016-04-04 10:56:44
• date last changed: 2024-01-30 10:28:42