A double-blind, placebo-controlled, cross-over study to establish the bifidogenic effect of a very-long-chain inulin extracted from globe artichoke (Cynara scolymus) in healthy human subjects

There is growing interest in the use of inulins as substrates for the selective growth of beneficial gut bacteria such as bifidobacteria and lactobacilli because recent studies have established that their prebiotic effect is linked to several health benefits. In the present study, the impact of a very-long-chain inulin (VLCI), derived from globe artichoke (Cynara scolymus), on the human intestinal microbiota compared with maltodextrin was determined. A double-blind, cross-over study was carried out in thirty-two healthy adults who were randomised into two groups and consumed 10 g/d of either VLCI or maltodextrin, for two 3-week study periods, separated by a 3-week washout period. Numbers of faecal bifidobacteria and lactobacilli were significantly higher upon VLCI ingestion compared with the placebo. Additionally, levels of Atopobium group significantly increased, while Bacteroides–Prevotella numbers were significantly reduced. No significant changes in faecal SCFA concentrations were observed. There were no adverse gastrointestinal symptoms apart from a significant increase in mild and moderate bloating upon VLCI ingestion. These observations were also confirmed by in vitro gas production measurements. In conclusion, daily consumption of VLCI extracted from globe artichoke exerted a pronounced prebiotic effect on the human faecal microbiota composition and was well tolerated by all volunteers.

[1]  W. Verstraete,et al.  Inulin‐type fructans of longer degree of polymerization exert more pronounced in vitro prebiotic effects , 2007, Journal of applied microbiology.

[2]  G. Gibson,et al.  The prebiotic effects of biscuits containing partially hydrolysed guar gum and fructo-oligosaccharides – a human volunteer study , 2001, British Journal of Nutrition.

[3]  B. Stahl,et al.  Dosage-Related Bifidogenic Effects of Galacto- and Fructooligosaccharides in Formula-Fed Term Infants , 2002, Journal of pediatric gastroenterology and nutrition.

[4]  D. Meyer,et al.  A double-blind placebo-controlled study to establish the bifidogenic dose of inulin in healthy humans , 2007, European Journal of Clinical Nutrition.

[5]  G R Gibson,et al.  Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. , 1995, The Journal of nutrition.

[6]  H. Englyst,et al.  Prebiotic digestion and fermentation. , 2001, The American journal of clinical nutrition.

[7]  P. Shewry,et al.  In vitro fermentation by human fecal microflora of wheat arabinoxylans. , 2007, Journal of agricultural and food chemistry.

[8]  M. Blaut,et al.  Effects of inulin on faecal bifidobacteria in human subjects , 1999, British Journal of Nutrition.

[9]  M. Theodorou,et al.  Comparison of bovine rumen liquor and bovine faeces as inoculum for an in vitro gas production technique for evaluating forages , 2001 .

[10]  M. Blaut,et al.  Effects of inulin and lactose on fecal microflora, microbial activity, and bowel habit in elderly constipated persons. , 1997, The American journal of clinical nutrition.

[11]  Wendy K.W. Yap,et al.  Changes in Infants Faecal Characteristics and Microbiota by Inulin Supplementation , 2008, Journal of clinical biochemistry and nutrition.

[12]  G. Gibson,et al.  In vitro fermentation of carbohydrates by porcine faecal inocula and their influence on Salmonella Typhimurium growth in batch culture systems. , 2008, FEMS microbiology ecology.

[13]  H. Haenel W. Ries: Methoden und Erkenntnisse der Alternsforschung. Sitzungsberichte der Sächsischen Akademie der Wissenschaften zu Leipzig. Math.-nat. Klasse, Bd. 119, Heft 1. 30 Seiten, 19 Abb. Akademie-Verlag, Berlin 1986. Preis: 4,— M , 1987 .

[14]  M. Roberfroid,et al.  Functional food science and gastrointestinal physiology and function , 1998, British Journal of Nutrition.

[15]  J. Hautvast,et al.  Effect of transgalactooligosaccharides on the composition of the human intestinal microflora and on putative risk markers for colon cancer. , 1999, The American journal of clinical nutrition.

[16]  F. Bornet,et al.  Short-chain fructo-oligosaccharide administration dose-dependently increases fecal bifidobacteria in healthy humans. , 1999, The Journal of nutrition.

[17]  J. Van Loo,et al.  On the presence of inulin and oligofructose as natural ingredients in the western diet. , 1995, Critical reviews in food science and nutrition.

[18]  N. J. Chatterton,et al.  Science and Technology of Fructans , 1993 .

[19]  G. Gibson,et al.  Gastrointestinal microflora: probiotics. , 2006, Advances in applied microbiology.

[20]  H. Harmsen,et al.  Extensive Set of 16S rRNA-Based Probes for Detection of Bacteria in Human Feces , 2002, Applied and Environmental Microbiology.

[21]  M. Wilkinson,et al.  Quantitative fluorescence in situ hybridization of Bifidobacterium spp. with genus-specific 16S rRNA-targeted probes and its application in fecal samples , 1995, Applied and environmental microbiology.

[22]  Masaki Ito,et al.  Effects of Administration of Galactooligosaccharides on the Human Faecal Microflora, Stool Weight and Abdominal Sensation , 1990 .

[23]  G. Holtrop,et al.  Effect of inulin on the human gut microbiota: stimulation of Bifidobacterium adolescentis and Faecalibacterium prausnitzii , 2008, British Journal of Nutrition.

[24]  M. Roberfroid Prebiotics: the concept revisited. , 2007, The Journal of nutrition.

[25]  G. Schaafsma,et al.  Nondigestible oligosaccharides do not interfere with calcium and nonheme-iron absorption in young, healthy men. , 1998, The American journal of clinical nutrition.

[26]  R. Buddington,et al.  Influence of Dietary Neosugar on Selected Bacterial Groups of the Human Faecal Microbiota , 1994 .

[27]  H. Jacobs,et al.  Digestive tolerance of inulin-type fructans: a double-blind, placebo-controlled, cross-over, dose-ranging, randomized study in healthy volunteers , 2009, International journal of food sciences and nutrition.

[28]  M. Roberfroid,et al.  Dietary modulation of the human colonic microbiota: updating the concept of prebiotics , 2004, Nutrition Research Reviews.

[29]  M. Blaut Relationship of prebiotics and food to intestinal microflora , 2002, European journal of nutrition.

[30]  B. Stahl,et al.  Supplementation of a bovine milk formula with an oligosaccharide mixture increases counts of faecal bifidobacteria in preterm infants , 2002, Archives of disease in childhood. Fetal and neonatal edition.

[31]  G R Gibson,et al.  Selective stimulation of bifidobacteria in the human colon by oligofructose and inulin. , 1995, Gastroenterology.

[32]  P. Coussement Inulin and oligofructose: safe intakes and legal status. , 1999, The Journal of nutrition.

[33]  B. Geypens,et al.  EFFECT OF HIGH PERFORMANCE CHICORY INULIN ON CONSTIPATION , 2000 .

[34]  Gerwin C. Raangs,et al.  Variations of Bacterial Populations in Human Feces Measured by Fluorescent In Situ Hybridization with Group-Specific 16S rRNA-Targeted Oligonucleotide Probes , 1998, Applied and Environmental Microbiology.

[35]  R. Beck,et al.  Determination of fructan oligomers of degree of polymerization 2–30 by high-performance liquid chromatography , 1984 .

[36]  J. Dijkstra,et al.  Estimating the extent of degradation of ruminant feeds from a description of their gas production profiles observed in vitro: derivation of models and other mathematical considerations. , 2000, The British journal of nutrition.

[37]  H. Flint,et al.  pH and Peptide Supply Can Radically Alter Bacterial Populations and Short-Chain Fatty Acid Ratios within Microbial Communities from the Human Colon , 2005, Applied and Environmental Microbiology.

[38]  R. Beck,et al.  New high-performance gel permeation chromatographic system for the determination of low-molecular-weight amyloses , 1987 .

[39]  G. Gibson,et al.  Prebiotic effect of fruit and vegetable shots containing Jerusalem artichoke inulin: a human intervention study. , 2010, The British journal of nutrition.

[40]  L. Willmitzer,et al.  Transgenic potato (Solanum tuberosum) tubers synthesize the full spectrum of inulin molecules naturally occurring in globe artichoke (Cynara scolymus) roots. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[41]  R. Buddington,et al.  Dietary supplement of neosugar alters the fecal flora and decreases activities of some reductive enzymes in human subjects. , 1996, The American journal of clinical nutrition.

[42]  G. Macfarlane,et al.  Validation of a Three-Stage Compound Continuous Culture System for Investigating the Effect of Retention Time on the Ecology and Metabolism of Bacteria in the Human Colon , 1998, Microbial Ecology.

[43]  B. Flourié,et al.  Gastrointestinal tolerance to an inulin-rich soluble roasted chicory extract after consumption in healthy subjects. , 2010, Nutrition.

[44]  T. Takizawa,et al.  Effects of Fructooligosaccharides on Intestinal Flora and Human Health , 1986 .

[45]  M. Roberfroid,et al.  The bifidogenic nature of chicory inulin and its hydrolysis products. , 1998, The Journal of nutrition.

[46]  F. Brighenti,et al.  Effect of consumption of a ready-to-eat breakfast cereal containing inulin on the intestinal milieu and blood lipids in healthy male volunteers , 1999, European Journal of Clinical Nutrition.

[47]  R. Amann,et al.  Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations , 1990, Applied and environmental microbiology.

[48]  T. Mitsuoka,et al.  Effect of fructo-oligosaccharides on intestinal microflora. , 1987, Die Nahrung.

[49]  H. Harmsen,et al.  A 16S rRNA-targeted Probe for Detection of Lactobacilli and Enterococci in Faecal Samples by Fluorescent In Situ Hybridization , 1999 .

[50]  H. Flint,et al.  Selective colonization of insoluble substrates by human faecal bacteria. , 2007, Environmental microbiology.

[51]  F. Bornet,et al.  The capacity of short-chain fructo-oligosaccharides to stimulate faecal bifidobacteria: a dose-response relationship study in healthy humans , 2006, Nutrition journal.

[52]  T. Henle,et al.  Jerusalem artichoke and chicory inulin in bakery products affect faecal microbiota of healthy volunteers , 2007, British Journal of Nutrition.

[53]  S. A. Raccuia,et al.  Cynara cardunculus L., a potential source of inulin in the Mediterranean environment: screening of genetic variability , 2004 .

[54]  R. Rastall,et al.  Prebiotics and synbiotics: towards the next generation. , 2002, Current opinion in biotechnology.

[55]  R Amann,et al.  Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum cytophaga-flavobacter-bacteroides in the natural environment. , 1996, Microbiology.

[56]  G. Gibson,et al.  In vitro evaluation of the fermentation properties and potential prebiotic activity of Agave fructans , 2009, Journal of applied microbiology.

[57]  C. Andrieux,et al.  Comparative study of the fermentative characteristics of inulin and different types of fibre in rats inoculated with a human Whole faecal flora , 1995, British Journal of Nutrition.

[58]  G. Gibson,et al.  Polydextrose, Lactitol, and Fructo-Oligosaccharide Fermentation by Colonic Bacteria in a Three-Stage Continuous Culture System , 2004, Applied and Environmental Microbiology.

[59]  H. Harmsen,et al.  Development of 16S rRNA-Based Probes for theCoriobacterium Group and the Atopobium Cluster and Their Application for Enumeration of Coriobacteriaceaein Human Feces from Volunteers of Different Age Groups , 2000, Applied and Environmental Microbiology.

[60]  M. Theodorou,et al.  A semi-automated in vitro gas production technique for ruminant feedstuff evaluation , 1999 .

[61]  J. Knol,et al.  Colon Microflora in Infants Fed Formula with Galacto- and Fructo-Oligosaccharides: More Like Breast-Fed Infants , 2005, Journal of pediatric gastroenterology and nutrition.

[62]  G. Gibson,et al.  Prebiotic capacity of inulin-type fructans. , 2007, The Journal of nutrition.