Article pubs.acs.org/JAFC
Effects of Soluble and Insoluble Fractions from Bilberries, Black Currants, and Raspberries on Short-Chain Fatty Acid Formation, Anthocyanin Excretion, and Cholesterol in Rats Greta Jakobsdottir,*,† Ulf Nilsson,† Narda Blanco,‡ Olov Sterner,‡ and Margareta Nyman† †
Applied Nutrition and Food Chemistry, Department of Food Technology, Engineering and Nutrition, Kemicentrum, Lund University, P.O. Box 124, SE-221 00 Lund, Sweden ‡ Centre for Analysis and Synthesis, Department of Chemistry, Kemicentrum, Lund University, P.O. Box 124, SE-221 00 Lund, Sweden S Supporting Information *
ABSTRACT: Dietary fiber and flavonoids, important components in berries, are suggested to improve metabolic health. This study investigates whether soluble and insoluble fractions isolated from bilberry, black currant, and raspberry affect the formation of short-chain fatty acids (SCFAs), uptake and excretion of flavonoids, and levels of cholesterol differently. Cecal SCFA pools were higher in rats fed the soluble than the insoluble fractions (525 vs 166 μmol, P < 0.001), whereas higher concentrations of butyric acid were found in the distal colon and serum of rats fed the insoluble fractions (5 vs 3 μmol/g and 58 vs 29 μmol/L, respectively, P < 0.001). The soluble bilberry fraction gave lower amounts of liver cholesterol (56 mg) than the other berry fractions (87 ± 5 mg), formed the highest amount of SCFAs (746 vs 266 ± 21 μmol), and contributed the highest intake of anthocyanins. Cyanidin-3-glucoside monoglucuronide was detected in the urine of all groups, whereas anthocyanins were found only in groups fed soluble black currant and raspberry. KEYWORDS: berries, fiber, SCFAs, anthocyanins, cholesterol
■
INTRODUCTION Berries are known to be an important part of a healthy diet and a good source of many vitamins and minerals. Many other imperative compounds can be found in berries, such as dietary fiber and flavonoids.1 Dietary fibers have been connected to many positive health effects: they help in weight loss and appetite regulation and can reduce the risk of developing diseases such as type 2 diabetes and heart disease.2−4 The flavonoids are not essential to humans, but the health benefits of berries are often related to these components, and through their antioxidative capacity they may have a protective role against various diseases associated with oxidative stress.1,5 More than 4000 flavonoids have been described, and anthocyanins are a common group of flavonoids. Anthocyanins are found in high amounts in bilberries and black currants, whereas raspberries contain relatively low amounts, and they are responsible for the color of fruit and berry.6,7 Bilberries also contain high amounts of proanthocyanidins and raspberries, ellagitannins, whereas black currants contain only small amounts of these components.8 The bioavailability of various flavonoids is an important question in this respect. Dietary fibers are not digested in the small intestine, but reach the large intestine, where microbial fermentation takes place.2 Some fibers are also resistant to microbial degradation. The fermentation gives rise to short-chain fatty acids (SCFAs), mainly acetic, propionic, and butyric acids. The amount of SCFAs formed is dependent upon a number of factors, for example, the kind of dietary fiber that reaches the colon, the transit time, and the microbiota composition.9,10 Some SCFAs have been shown to have positive health effects, and butyric © 2014 American Chemical Society
acid has been mostly emphasized, but propionic may also have some interesting effects.11 Butyric acid is an energy source for the colonic epithelial cells,12 and impaired butyric acid metabolism has been associated with colonic diseases but also connected to decreased risk of metabolic diseases.13,14 The physicochemical properties of the dietary fiber, such as solubility, are important for the health-promoting effects and the formation of SCFAs.15 Very few studies have been focused on dietary fiber in berries. Some phenolic compounds, such as the flavonoids, may be absorbed in the small intestine after cleavage by intestinal esterases. The flavonoids can also be more or less tightly bound to the dietary fiber complex, which affects the bioavailability of these components.16,17 Depending on how they are associated with the dietary fiber, the substances may be released throughout the gut, and the specific physiological activity can vary on the basis of the site of release. Like the dietary fiber per se, another fraction of the flavonoids may be resistant to colonic degradation, thereby reaching feces intact and having no biological effect. Interest in new food components with prebiotic properties is growing. Many byproducts are formed during, for example, juice production. To get an idea of where the flavonoids in berries are located, and also which fibers are most active, we Received: Revised: Accepted: Published: 4359
September 4, 2013 April 14, 2014 April 27, 2014 May 5, 2014 dx.doi.org/10.1021/jf5007566 | J. Agric. Food Chem. 2014, 62, 4359−4368
Journal of Agricultural and Food Chemistry
Article
Table 1. Composition of Test Diets (g/kg, dwb) soluble bilberry casein
insoluble
black currant
raspberry
bilberry
black currant
raspberry
corn oil mineral mixturea vitamin mixtureb choline chloride berriesc sucrose wheat starchd
120 1.2 50 48 8 2 771 0 0
120 1.2 50 48 8 2 771 0 0
120 1.2 50 48 8 2 771 0 0
120 1.2 50 48 8 2 77 100 594
120 1.2 50 48 8 2 108 100 563
120 1.2 50 48 8 2 97 100 574
energy content (kJ/kg)
16600
16500
16400
16500
16400
16300
DL-methionine
Containing (g/kg) 0.43 CuSO4·5H2O, 1.6 ZnSO4·7H2O, 389 KH2PO4, 201.2 NaH2PO4·2H2O, 380 CaCO3, 0.08 KI, 67 MgSO4, 9 FeSO4·7H2O, 4 MnSO4·H2O, 0.023 CoCl·6H2O, 119.1 NaCl, 0.019 chromium(III)chloride, and 0.013 sodium selenate (Lantmännen AB, Sweden). bContaining (g/kg) 0.62 menadione, 2.5 thiamin hydrochloride, 2.5 riboflavin, 1.25 pyridoxine hydrochloride, 6.256 calcium pantothenate, 6.256 nicotinic acid, 0.25 folic acid, 12.5 inositol, 1.25 p-aminobenzoic acid, 0.05 biotin, 0.00375 cyanocobalamin, 0.187 retinol palmitate, 0.00613 calciferol (D3), 25 d-αtocopheryl acetate, and 941.25 maize starch (Lantmännen AB, Sweden). cCorresponding to 45 g dietary fiber/kg diet (dry weight basis) in diets containing bilberry and 60 g dietary fiber/kg diet (dry weight basis) in diets containing black currant and raspberry. The berries were from Procordia AB (Eslöv, Sweden). dNorfoods Sweden AB, Malmö, Sweden. a
Table 2. Composition and Fecal Excretion of Dietary Fiber in Rats Fed Soluble or Insoluble Fractions from Bilberry, Black Currant, or Raspberrya composition of dietary fiber soluble
dietary fiber polysaccharides (g/100 g, dwb) monomeric composition (%) rhamnose fucose arabinose xylose mannose galactose glucose uronic acid ligninb (g/100 g, dwb) total dietary fiber (g/100 g, dwb)
fecal excretion (%)
insoluble
soluble
insoluble
bilberry
black currant
raspberry
bilberry
black currant
raspberry
bilberry
black currant
raspberry
bilberry
black currant
raspberry
5.5c
3.4c
6.0c
18.2a
14.1b
18.5a
14bc
18bc
16bc
26a
11c
21ab
3 1 8 32a 5b 12 32b 7b
5 2 11 3c 9b 12 25b 33a
3 1 19a 7c 2b 13 26b 28a
1
