Elsevier

Journal of Functional Foods

Volume 34, July 2017, Pages 398-407
Journal of Functional Foods

Effects of potato dextrin on the composition and metabolism of the gut microbiota in rats fed standard and high-fat diets

https://doi.org/10.1016/j.jff.2017.05.023Get rights and content

Highlights

  • Dextrin stimulates the growth of strains Bacteroidetes and limited increase in Firmicutes.

  • The low-fat diet supplemented with dextrin increased total SCFAs.

  • The high-fat diet supplemented with dextrin reduced putrefactive processes.

  • Potato dextrin may prevent overweight and obesity.

Abstract

The objective of the study was to determine the influence of dextrin obtained from potato starch on the numbers and relative proportions of enteric bacteria belonging to the phyla Bacteroidetes, Actinobacteria, and Firmicutes. Moreover, basic indicators of gastrointestinal function and short-chain fatty acids were analyzed. Dextrin decreases feed consumption of rats and is intensively metabolized by bacteria in their distal intestine. Dextrin also reduces the level of putrefaction-related SCFAs in the distal intestine provided that it is consumed together with a high-fat diet; it also stimulates the growth of Bacteroidetes and Actinobacteria strains, while reducing the number of Firmicutes strains regardless of the dietary regimen. These results show that potato dextrin lowers feed intake and leads to modifications in the distal intestine which may help support intestinal health and prevent overweight and obesity.

Introduction

The gut microbiota plays a critical role in ensuring the correct functioning of the human body by affecting metabolic processes as well as immune and physiological functions (Neish, 2002, Nicholson et al., 2005, Stewart et al., 2004, Walker and Lawley, 2013). In recent years, there has been an increased interest in the contribution of enteric bacteria to the development of chronic diseases, such as obesity, type II diabetes mellitus, inflammatory bowel disease, and colonic cancer (Backhed et al., 2004, De Filippo et al., 2010, DuPont and DuPont, 2011, Feng et al., 2010, Tamboli et al., 2004, Tannock, 2008). Diet may significantly affect the etiology of those diseases as its composition may directly stimulate the growth of beneficial or unfavorable bacterial strains.

Colonization of the human gastrointestinal tract begins within hours of birth, but proceeds differently in different individuals. The gut microbiota in children is largely affected by the mode of delivery, the hospital environment, the manner of feeding, maternal and infant diseases, and medications administered to mother and child (Salminen & Isolauri, 2006). Initially, the gastrointestinal tract is colonized by a variety of Lactobacillus, Staphylococcus, Enterococcus, Escherichia, Enterobacter, Bifidobacterium, Bacteroides, Clostridium, and Eubacterium strains (Libudzisz et al., 2012, Moore et al., 2011). Intensive bacterial colonization of the human digestive system typically lasts until approximately two years of age, after which time the gut microbiota of the child becomes similar to that of an adult (Nowak & Libudzisz, 2008). The composition and relative content of bacteria undergoes major changes also in the elderly, with a significant reduction in Bacteroides and Bifidobacterium, and an increase in Clostridium, Eubacterium, and Fusobacterium strains. This change is linked to increasing pH of intestinal contents up to approximately 7.0–7.5, which may cause gastrointestinal disorders in seniors. The aforementioned childhood and old-age processes notwithstanding, the composition of intestinal microorganisms is rather stable in healthy adults and represents a climax community (Nowak & Libudzisz, 2008). Bacteroidetes and Firmicutes strains account for over 90% of the gut microbial population. The predominant bacterial genera include obligate anaerobes: Bacteroides, Eubacterium, Clostridium, Ruminococcus, Peptococcus, Peptostreptococcus, Bifidobacterium, and Fusobacterium, as well as facultative ones: Escherichia, Enterobacter, Enterococcus, Klebsiella, Proteus, and Lactobacillus (Shen, Obin, & Zhao, 2013).

A considerable body of research has shown that obesity is linked to major changes in the composition and metabolic function of the gut microbiota. Of particular importance are the relative proportions of Bacteroidetes and Firmicutes strains (Ley et al., 2006, Sanz and Santacruz, 2008). The research teams of Backhed, Gordon, and De Filippo have reported that the composition of intestinal microorganisms may contribute to human obesity (Backhed et al., 2004, De Filippo et al., 2010, Ley et al., 2006). Backhed et al., who determined the content of Bacteroidetes and Firmicutes strains in obese and normal mice, found that the relative proportion of Bacteroidetes was much lower in the former (20%), while in normal-weight mice those bacteria accounted for 40% of total microbial count (Backhed et al., 2007, Backhed et al., 2004). On the other hand, in the study by Fleissner mice fed a diet rich in animal fats and poor in dietary fiber exhibited lower numbers of Bacteroidetes strains and higher numbers of Firmicutes strains (Fleissner et al., 2010). A study of 12 obese individuals, some of whom received a low-fat diet and some a low-saccharide one, showed that Firmicutes and Bacteroidetes were the predominant phyla in both groups; however in the obese the proportion of Bacteroidetes amounted to only 1% to 5%, while in normal-weight individuals it was 20%. The consumption of a low-fat diet led to an increased content of Bacteroidetes strains and lower levels of Firmicutes strains (Ley et al., 2006). The research teams of Backhed, Gordon, and De Filippo have been confirmed by Verdam et al. (2013). Contradictory results have even been reported, a similar microbiota composition in lean and obese subjects (Duncan et al., 2008), an opposite change in Bacteroidetes/Firmicutes ratio in obesity (Schwiertz et al., 2010). These conflicting data may be attributable to factors such as recent use of antibiotics (Dethlefsen, Huse, Sogin, & Relman, 2008), different diet (Turnbaugh, Backhed, Fulton, & Gordon, 2008), host physiology (Benson et al., 2010), or the presence of obesity associated comorbidity such as insulin re-sistance (Larsen et al., 2010).

Fiber preparations and other indigestible polysaccharides are not hydrolyzed and absorbed in the upper part of the gastrointestinal tract, and so they reach the colon in unaltered form, where they provide nutrients for beneficial bacteria. They constitute a promising means of modulating the intestinal microbiota and may possess prebiotic properties; therefore, it has been suggested that they should be included in the human diet (FAO Technical Meeting on Prebiotics, 2007, Louis et al., 2007). Such polysaccharides encompass resistant dextrins, which are defined as short-chain, starch-derived polymers of glucose that are resistant to digestion in the human gastrointestinal tract (Ohkuma, Hanno, Inaba, Matsuda, & Katsuda, 1997). Studies on rats and healthy individuals have confirmed that prebiotics increase the feeling of satiety (Cani et al., 2007, Parnell and Reimer, 2009). The favorable effects of prebiotics on the gut microbiota are linked to SCFA production and increased levels of PYY (a peptide synthesized and secreted by ileal and colonic L cells which stimulates the satiety center) and GLP-1 (which reduces glycemia, insulin resistance, and adipose tissue mass, as well as stimulate the feeling of satiety) (Alvarez-Castro et al., 2012, Delzenne et al., 2011, Parnell et al., 2012).

The objective of the present study was to determine the effects of resistant dextrin from potato starch (prepared according to patent No P.392894 obtained by heating potato starch acidified with hydrochloric and citric acids at 130 °C for 4 h and previously physically, chemically characterized Barczynska, Slizewska, Litwin et al., 2015, Barczynska, Śliżewska, Libudzisz et al., 2015) using selected indicators of gastrointestinal function in rats following 12 weeks of administering a control diet (C) or a high-fat diet (HF) with or without dextrin (+PD). The work in particular focused on the composition of the gut microbiota, the content of bacteria belonging to the phyla Bacteroidetes, Actinobacteria, and Firmicutes, as well as the bacterial metabolites present in the distal intestine (short-chain fatty acids, SCFAs) and bacterial glycolytic activity. It was hypothesized that the replacement of insoluble fiber in the form of cellulose, which does not constitute an energy substrate for the intestinal bacteria, with resistant dextrin would bring about beneficial changes in the gut microbiota and could improve the basic indicators of gastrointestinal function in rats depending on the consumed diet (standard or high-fat).

Section snippets

Dextrin

The dextrin used in the study was produced at the Department of Biochemistry and Technology of Bioproducts, Jan Dlugosz University in Czestochowa. The dextrin was obtained according to patent No. P.392894 (Barczynska, Kapuśniak, Jochym, Śliżewska, & Libudzisz, 2015). Resistant citric acid-modified dextrin was prepared according to method of P.392894. Thus, potato starch was sprayed with a hydrochloric acid solution (0.5% w/w) to obtain a final HCl concentration of 0.1% on a dry starch basis

Results

After 12 weeks of the experiment, feed consumption was reduced both by the HF diet and by supplementation with potato dextrin (Table 3, P < 0.001 and P < 0.05, respectively). Nevertheless, due to its very high calorie content the HF diet significantly increased final body weight, weight gain, and epididymal fat mass in rats (P = 0.001, P = 0.001 and P < 0.05, respectively), while potato dextrin did not have a significant effect in that respect (P > 0.05). Both factors (diet and dextrin supplementation)

Discussion

The past several decades have seen a significant increase in the prevalence of obesity in adults and children alike. Indeed, this disorder has reached epidemic proportions around the world. The development of obesity is linked to both environmental and genetic factors. Recent research has shown that an important role in maintaining normal body weight is played by the gut microbiota. Thus, a strategy for containing obesity should involve the development of prebiotics/ingredients fermented by the

Conclusions

Dextrin obtained as a result of heating potato starch in the presence of hydrochloric acid as a catalyst and citric acid as a cross-linking agent at 130 °C for 240 min decreases feed consumption of rats and is intensively metabolized by bacteria in their distal intestine. Potato dextrin also reduces the level of putrefaction-related SCFAs in the distal intestine provided that it is consumed together with a high-fat diet; it also stimulates the growth of Bacteroidetes and Actinobacteria strains,

Acknowledgements

This project was funded by the National Science Centre allocated on the basis of the decision number DEC-2011/03/D/440 NZ9/03601.

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