Introduction. Berries contain high amounts of dietary fibre and flavonoids and have been associated with improved metabolic health. The mechanisms are not clear but the formation of SCFAs, especially propionic and butyric acids, could be important. The potent antioxidant and antimicrobial properties of flavonoids could also be a factor, but little is known about their fate in the gastrointestinal tract. Aim. To compare how blackcurrants, blackberries, raspberries, and Lactobacillus plantarum HEAL19 affect formation of SCFAs, inflammatory status, caecal microbial diversity, and flavonoids. Results and Conclusions. Degradation of the dietary fibre, formation of SCFAs including propionic and butyric acids, the weight of the caecal content and tissue, and the faecal wet and dry weight were all higher in rats fed blackcurrants rather than blackberries or raspberries. However, the microbial diversity of the gut microbiota was higher in rats fed raspberries. The high content of soluble fibre in blackcurrants and the high proportion of mannose-containing polymers might explain these effects. Anthocyanins could only be detected in urine of rats fed blackcurrants, and the excretion was lower with HEAL19. No anthocyanins or anthocyanidins were detected in caecal content or blood. This may indicate uptake in the stomach or small intestine. 1. Introduction Berries contain many bioactive compounds such as dietary fibre, phenolic acids, and flavonoids, which may have a number of nutritional properties [1, 2]. Berries and their flavonoids have received much attention in recent years, but little is known about the fate of the flavonoids in the body. Furthermore, few studies have examined dietary fibre in berries. Phenolic acids and flavonoids are phytochemicals common in berries, fruits, and vegetables that are a part of a daily diet and may be among their health-promoting factors [2]. Such compounds are also found in, for example, wine and tea. More than 4000 different flavonoids have been described. The dominating group of flavonoids in red berries is anthocyanins, which also predominate in blackcurrants and blueberries [3]. The anthocyanins belong to the flavonoid family and are responsible for the red, orange, and blue colours in fruits [4]. In epidemiological and clinical studies, berries have been associated with improved cardiovascular risk profiles [5] and high consumption of fruits and flavonoids is associated with reduced risk of cardiovascular diseases [3], cancer, coronary heart disease, stroke, and various chronic diseases [2, 6]. In addition to being
References
[1]
K. R. M？？tt？-Riihinen, A. Kamal-Eldin, P. H. Mattila, A. M. González-Paramás, and R. T？rr？nen, “Distribution and contents of phenolic compounds in eighteen scandinavian berry species,” Journal of Agricultural and Food Chemistry, vol. 52, no. 14, pp. 4477–4486, 2004.
[2]
G. Borges, A. Degeneve, W. Mullen, and A. Crozier, “Identification of flavonoid and phenolic antioxidants in black currants, blueberries, raspberries, red currants, and cranberries,” Journal of Agricultural and Food Chemistry, vol. 58, no. 7, pp. 3901–3909, 2010.
[3]
R. Puupponen-Pimi？, L. Nohynek, C. Meier et al., “Antimicrobial properties of phenolic compounds from berries,” Journal of Applied Microbiology, vol. 90, no. 4, pp. 494–507, 2001.
[4]
H. Wang, G. Cao, and R. L. Prior, “Oxygen radical absorbing capacity of anthocyanins,” Journal of Agricultural and Food Chemistry, vol. 45, no. 2, pp. 304–309, 1997.
[5]
A. Basu, M. Rhone, and T. J. Lyons, “Berries: emerging impact on cardiovascular health,” Nutrition Reviews, vol. 68, no. 3, pp. 168–177, 2010.
[6]
L. W. Morton, R. A.-A. Caccetta, I. B. Puddey, and K. D. Croft, “Chemistry and biological effects of dietary phenolic compounds: relevance to cardiovascular disease,” Clinical and Experimental Pharmacology and Physiology, vol. 27, no. 3, pp. 152–159, 2000.
[7]
Y. S. Velioglu, G. Mazza, L. Gao, and B. D. Oomah, “Antioxidant activity and total phenolics in selected fruits, vegetables, and grain products,” Journal of Agricultural and Food Chemistry, vol. 46, no. 10, pp. 4113–4117, 1998.
[8]
J. W. Anderson, P. Baird, R. H. Davis Jr. et al., “Health benefits of dietary fiber,” Nutrition Reviews, vol. 67, no. 4, pp. 188–205, 2009.
[9]
J. M. Wong and D. J. Jenkins, “Carbohydrate digestibility and metabolic effects,” Journal of Nutrition, vol. 137, no. 11, supplement, pp. 2539S–2546S, 2007.
[10]
N. I. McNeil, J. H. Cummings, and W. P. T. James, “Short chain fatty acid absorption by the human large intestine,” Gut, vol. 19, no. 9, pp. 819–822, 1978.
[11]
J. M. W. Wong, R. De Souza, C. W. C. Kendall, A. Emam, and D. J. A. Jenkins, “Colonic health: fermentation and short chain fatty acids,” Journal of Clinical Gastroenterology, vol. 40, no. 3, pp. 235–243, 2006.
[12]
S. I. Cook and J. H. Sellin, “Review article: short chain fatty acids in health and disease,” Alimentary Pharmacology and Therapeutics, vol. 12, no. 6, pp. 499–507, 1998.
[13]
J. H. Cummings, M. J. Hill, and E. S. Bone, “The effect of meat protein and dietary fiber on colonic function and metabolism. II. Bacterial metabolites in feces and urine,” American Journal of Clinical Nutrition, vol. 32, no. 10, pp. 2094–2101, 1979.
[14]
C. Br？nning, ？. H？kansson, S. Ahrné, B. Jeppsson, G. Molin, and M. Nyman, “Blueberry husks and multi-strain probiotics affect colonic fermentation in rats,” British Journal of Nutrition, vol. 101, no. 6, pp. 859–870, 2009.
[15]
K. E. Bach Knudsen, A. Serena, N. Canibe, and K. S. Juntunen, “New insight into butyrate metabolism,” Proceedings of the Nutrition Society, vol. 62, no. 1, pp. 81–86, 2003.
[16]
G. T. Macfarlane and S. Macfarlane, “Bacteria, colonic fermentation, and gastrointestinal health,” Journal of AOAC International, vol. 95, no. 1, pp. 50–60, 2012.
[17]
J.-P. Segain, J.-P. Galmiche, D. Raingeard De La Blétière et al., “Butyrate inhibits inflammatory responses through NFκB inhibition: implications for Crohn's disease,” Gut, vol. 47, no. 3, pp. 397–403, 2000.
[18]
P. Rosignolli, R. Fabianni, A. De Bartolomeo et al., “Protective activity of butyrate on hydrogen peroxide-induced DNA damage in isolated human colonocytes and HT29 tumour cells,” Carcinogenesis, vol. 22, no. 10, pp. 1675–1680, 2001.
[19]
I. A. Finnie, A. D. Dwarakanath, B. A. Taylor, and J. M. Rhodes, “Colonic mucin synthesis is increased by sodium butyrate,” Gut, vol. 36, no. 1, pp. 93–99, 1995.
[20]
W. Scheppach, H. P. Bartram, and F. Richter, “Role of short-chain fatty acids in the prevention of colorectal cancer,” European Journal of Cancer Part A, vol. 31, no. 7-8, pp. 1077–1080, 1995.
[21]
D. Topping, “Cereal complex carbohydrates and their contribution to human health,” Journal of Cereal Science, vol. 46, no. 3, pp. 220–229, 2007.
[22]
T. Asano and R. S. McLeod, “Dietary fibre for the prevention of colorectal adenomas and carcinomas,” Cochrane Database of Systematic Reviews, no. 2, Article ID CD003430, 2002.
[23]
M. O. Weickert and A. F. H. Pfeiffer, “Metabolic effects of dietary fiber consumption and prevention of diabetes,” Journal of Nutrition, vol. 138, no. 3, pp. 439–442, 2008.
[24]
D. J. Rose, M. T. DeMeo, A. Keshavarzian, and B. R. Hamaker, “Influence of dietary fiber on inflammatory bowel disease and colon cancer: importance of fermentation pattern,” Nutrition Reviews, vol. 65, no. 2, pp. 51–62, 2007.
[25]
G. Molin, “Probiotics in foods not containing milk or milk constituents, with special reference to Lactobacillus plantarum 299v,” American Journal of Clinical Nutrition, vol. 73, no. 2, pp. 380S–385S, 2001.
[26]
G. Molin, Lactobacillus Plantarum HEAL 19, Probi, Lund, Sweden, 2013.
[27]
N. Osman, D. Adawi, S. Ahrné, B. Jeppsson, and G. Molin, “Probiotics and blueberry attenuate the severity of dextran sulfate sodium (DSS)-induced colitis,” Digestive Diseases and Sciences, vol. 53, no. 9, pp. 2464–2473, 2008.
[28]
C. Rask, I. Adlerberth, A. Berggren, et al., “Differential effect on cell-mediated immunity in human volunteers after intake of different lactobacilli,” Clinical and Experimental Immunology, vol. 172, no. 2, pp. 321–332, 2013.
[29]
M. Nyman and N. G. Asp, “Fermentation of dietary fibre components in the rat intestinal tract,” British Journal of Nutrition, vol. 47, no. 3, pp. 357–366, 1982.
[30]
I. Bjorck, E. M. Nyman, B. Pedersen, et al., “Formation of enzyme resistant starch during autoclaving of wheat starch: studies in vitro and in vivo,” Journal of Cereal Science, vol. 6, no. 2, pp. 159–172, 1987.
[31]
H. Hilz, E. J. Bakx, H. A. Schols, and A. G. J. Voragen, “Cell wall polysaccharides in black currants and bilberries—characterisation in berries, juice, and press cake,” Carbohydrate Polymers, vol. 59, no. 4, pp. 477–488, 2005.
[32]
G. Zhao, J.-F. Liu, M. Nyman, and J. ？. J？nsson, “Determination of short-chain fatty acids in serum by hollow fiber supported liquid membrane extraction coupled with gas chromatography,” Journal of Chromatography B, vol. 846, no. 1-2, pp. 202–208, 2007.
[33]
O. Theander, P. Aman, E. Westerlund, R. Andersson, and D. Pettersson, “Total dietary fiber determined as neutral sugar residues, uronic acid residues, and Klason lignin (the Uppsala method): collaborative study,” Journal of AOAC International, vol. 78, no. 4, pp. 1030–1044, 1995.
[34]
G. Zhao, M. Nyman, and J. ？. J？nsson, “Rapid determination of short-chain fatty acids in colonic contents and faeces of humans and rats by acidified water-extraction and direct-injection gas chromatography,” Biomedical Chromatography, vol. 20, no. 8, pp. 674–682, 2006.
[35]
K. M？？tt？, A. Kamal-Eldin, and R. T？rr？nen, “Phenolic compounds in berries of black, red, green, and white currants (Ribes sp.),” Antioxidants and Redox Signaling, vol. 3, no. 6, pp. 981–993, 2001.
[36]
K. Ogawa, H. Sakakibara, R. Iwata et al., “Anthocyanin composition and antioxidant activity of the crowberry (Empetrum nigrum) and other berries,” Journal of Agricultural and Food Chemistry, vol. 56, no. 12, pp. 4457–4462, 2008.
[37]
U. Axling, C. Olsson, J. Xu, et al., “Green tea powder and Lactobacillus plantarum affect gut microbiota, lipid metabolism and inflammation in high-fat fed C57BL/6J mice,” Nutrition and Metabolism, vol. 9, no. 1, p. 105, 2012.
[38]
？. M. Henningsson, I. M. E. Bj？rck, and E. M. G. L. Nyman, “Combinations of indigestible carbohydrates affect short-chain fatty acid formation in the hindgut of rats,” Journal of Nutrition, vol. 132, no. 10, pp. 3098–3104, 2002.
[39]
T. C. Rideout, S. V. Harding, P. J. H. Jones, and M. Z. Fan, “Guar gum and similar soluble fibers in the regulation of cholesterol metabolism: current understandings and future research priorities,” Vascular Health and Risk Management, vol. 4, no. 5, pp. 1023–1033, 2008.
[40]
A. Nilsson, K. Radeborg, and I. Bjorck, “Effects on cognitive performance of modulating the postprandial blood glucose profile at breakfast,” European Journal of Clinical Nutrition, vol. 66, no. 9, pp. 1039–1043, 2012.
[41]
A. Lazaridou and C. G. Biliaderis, “Molecular aspects of cereal β-glucan functionality: physical properties, technological applications and physiological effects,” Journal of Cereal Science, vol. 46, no. 2, pp. 101–118, 2007.
[42]
T. Immerstrand, Cholesterol-lowering properties of oats: effects of processing and the role of oat components [Dissertation], Lund University, 2010.
[43]
T. Immerstrand, K. E. Andersson, C. Wange et al., “Effects of oat bran, processed to different molecular weights of beta;-glucan, on plasma lipids and caecal formation of SCFA in mice,” British Journal of Nutrition, vol. 104, no. 3, pp. 364–373, 2010.
[44]
G. Annison and D. L. Topping, “Nutritional role of resistant starch: chemical structure vs physiological function,” Annual Review of Nutrition, vol. 14, pp. 297–320, 1994.
[45]
G. M. Wyatt, N. Horn, J. M. Gee, and I. T. Johnson, “Intestinal microflora and gastrointestinal adaptation in the rat in response to non-digestible dietary polysaccharides,” British Journal of Nutrition, vol. 60, no. 2, pp. 197–207, 1988.
[46]
M. ？. Henningsson, Content and distribution of short-chain fatty acids in the hindgut of rats fed various sources of indigestible carbohydrates [Dissertation], Lund University, 2002.
[47]
P. J. Turnbaugh, M. Hamady, T. Yatsunenko et al., “A core gut microbiome in obese and lean twins,” Nature, vol. 457, no. 7228, pp. 480–484, 2009.
[48]
L. K. Ursell, J. C. Clemente, J. R. Rideout, D. Gevers, J. G. Caporaso, and R. Knight, “The interpersonal and intrapersonal diversity of human-associated microbiota in key body sites,” Journal of Allergy and Clinical Immunology, vol. 129, no. 5, pp. 1204–1208, 2012.
[49]
？. H？kansson, C. Br？nning, G. Molin et al., “Blueberry husks and probiotics attenuate colorectal inflammation and oncogenesis, and liver injuries in rats exposed to cycling DSS-treatment,” PLoS ONE, vol. 7, no. 3, Article ID e33510, 2012.
[50]
R. Osawa, K. Kuroiso, S. Goto, and A. Shimizu, “Isolation of tannin-degrading lactobacilli from humans and fermented foods,” Applied and Environmental Microbiology, vol. 66, no. 7, pp. 3093–3097, 2000.
[51]
J. Serrano, R. Puupponen-Pimi？, A. Dauer, A.-M. Aura, and F. Saura-Calixto, “Tannins: current knowledge of food sources, intake, bioavailability and biological effects,” Molecular Nutrition and Food Research, vol. 53, no. 2, pp. S310–S329, 2009.
[52]
R. Puupponen-Pimi？, L. Nohynek, S. Hartmann-Schmidlin et al., “Berry phenolics selectively inhibit the growth of intestinal pathogens,” Journal of Applied Microbiology, vol. 98, no. 4, pp. 991–1000, 2005.
[53]
N. P. Seeram, “Berry fruits: compositional elements, biochemical activities, and the impact of their intake on human health, performance, and disease,” Journal of Agricultural and Food Chemistry, vol. 56, no. 3, pp. 627–629, 2008.
[54]
M. Heinonen, “Antioxidant activity and antimicrobial effect of berry phenolics—a Finnish perspective,” Molecular Nutrition and Food Research, vol. 51, no. 6, pp. 684–691, 2007.
[55]
T. Siriwoharn, R. E. Wrolstad, C. E. Finn, and C. B. Pereira, “Influence of cultivar, maturity, and sampling on blackberry (Rubus L. hybrids) anthocyanins, polyphenolics, and antioxidant properties,” Journal of Agricultural and Food Chemistry, vol. 52, no. 26, pp. 8021–8030, 2004.
[56]
A. Scalbert, “Antimicrobial properties of tannins,” Phytochemistry, vol. 30, no. 12, pp. 3875–3883, 1991.
[57]
T. De Bruyne, L. Pieters, H. Deelstra, and A. Vlietinck, “Condensed vegetable tannins: biodiversity in structure and biological activities,” Biochemical Systematics and Ecology, vol. 27, no. 4, pp. 445–459, 1999.
[58]
M. Jakesevic, K. Aaby, G.-I. A. Borge, B. Jeppsson, S. Ahrné, and G. Molin, “Antioxidative protection of dietary bilberry, chokeberry and Lactobacillus plantarum HEAL19 in mice subjected to intestinal oxidative stress by ischemia-reperfusion,” BMC Complementary and Alternative Medicine, vol. 11, article 8, 2011.
[59]
J. He and M. M. Giusti, “Anthocyanins: natural colorants with health-promoting properties,” Annual Review of Food Science and Technology, vol. 1, pp. 163–187, 2010.
[60]
L. Utsal, V. Tillmann, M. Zilmer, et al., “Elevated serum IL-6, IL-8, MCP-1, CRP, and IFN-gamma levels in 10- to 11-year-old boys with increased BMI,” Hormone Research in Paediatrics, vol. 78, no. 1, pp. 31–39, 2012.
[61]
Z. H. Liu, L. L. Chen, X. L. Deng, et al., “Methylation status of CpG sites in the MCP-1 promoter is correlated to serum MCP-1 in Type 2 diabetes,” Journal of Endocrinological Investigation, vol. 35, no. 6, pp. 585–589, 2012.
