Elsevier

Journal of Functional Foods

Volume 17, August 2015, Pages 189-201
Journal of Functional Foods

Prebiotics, gut microbiota and metabolic risks: Unveiling the relationship

https://doi.org/10.1016/j.jff.2015.05.004Get rights and content

Highlights

  • Gut infections are still one of the major causes of ailments.

  • Dietary oligosaccharides have potential to modulate intestinal infections.

  • Protective mechanisms of prebiotics includes modulation of gut microbiota and changes in inflammatory response.

  • The potential of prebiotics against physiological threats is documented by various animals and human studies.

Abstract

The human gastrointestinal tract is colonized by trillions of microbes comprising thousands of bacterial phylotypes. Recent metagenomic studies of the human gut microbiota have revealed the presence of millions of genes, as compared to genes present in the entire human body. Perturbation in the level of gut microorganisms may lead to the onset of metabolic disorders. However, compelling evidence has also suggested that a particular gut microbial community may halt the occurrence of metabolic risk factors. Restoration of the beneficial gut microbial balance is difficult to achieve but the exploitation of prebiotics has led to promising outcomes in various studies.

Introduction

Prebiotics are non-digestible food components that selectively stimulate the growth or activity of specific indigenous bacteria in the digestive tract in a manner claimed to be beneficial for the host. They were identified in the early 1950s by Gyorgy (1953) as “bifidus factor,” a bifidogenic substance that selectively improved the growth of bifidobacteria. The term prebiotic was first devised in 1995 by Gibson and co-workers (Gibson, Roberfroid, 1995, Sharma et al, 2012). Earlier work on prebiotics only elaborated on the microbial changes in the human digestive ecosystem. Later work provided evidence that prebiotics allow desirable changes in the composition as well as the activity of the gastrointestinal microflora and confer health benefits to the host (Kanakupt et al, 2011, Nagpal et al, 2014).

Prebiotics are primarily carbohydrates (oligosaccharides and polysaccharides), but may include some non-carbohydrate moieties. Soluble fibres are the most prevailing type of prebiotics. Nevertheless, various other forms of dietary fibre may serve the purpose. In this context, criteria have been established to categorize any food ingredient as a candidate prebiotics: they have the ability to resist gastric hydrolysis by digestive enzymes and remain unabsorbed in the upper gastrointestinal tract; they undergo fermentation by resident microbiota in the large intestine; and they stimulate the activity/growth of potentially beneficial intestinal bacteria (Xiao et al, 2014, Yeo et al, 2009).

Mechanistically, prebiotics are non-viable food constituents having pronounced effect on human health by modulating colonic microflora (FAO, 2007). They induce specific changes in the composition of gut microbiota, increase the number of bifidobacteria and lactobacilli. Alongside, prebiotics decrease the toxin-producing bacteria like bacteroides, proteolytic clostridia and Escherichia coli (Ogueke, Owuamanam, Ihediohanma, & Iwouno, 2010). According to the criteria, many non-digestible food oligosaccharides exhibit prebiotic activities. Likewise, fructooligosaccharides, xylooligosaccharides, isomaltooligosaccharides and glucooligosaccharides as well as some sugar alcohols and polysaccharides (modified and resistant starch) are also included in this category. They can either be produced enzymatically or found naturally in some plants (Cummings, Macfarlane, & Englyst, 2001).

The promising health benefits associated with prebiotics are improvement in the gastrointestinal microflora, enhanced mineral absorption, stimulation of the immune system, reduced risk of irritable bowel syndrome and of constipation (Gibson, Probert, van Loo, Rastall, & Roberfroid, 2004). They also prevent colorectal cancer and exhibit cholesterol lowering potential (Kelly, 2003). Nevertheless, the health enhancing effects of prebiotics are not direct as they selectively nourish the microbial community i.e. lactobacilli and bifidobacteria that in turn improve gut health. Approximately 300 to 500 species of bacteria occur in the human gastrointestinal tract that becomes denser in the large intestine, approaching a concentration of microbial cells 1011/g of luminal content (Guarner & Malagelada, 2003). It has been established that almost 55% of faecal bulk consists of microorganisms. The microbial colonization in the digestive tract is markedly influenced by transit time and luminal pH (Paineau et al., 2008).

The majority of colon bacteria are anaerobes that avail energy through fermentation. In this context, main fermentative substrates from dietary source are non-digestible carbohydrates i.e. oligosaccharides, fibres, resistant starches and non-starch polysaccharides that escape digestion in the small intestine. Nonetheless, carbohydrate fermentation products are effective substrates leading to gradient utilization by the colon (Macfarlane, Steed, & Macfarlane, 2008). The ascending colon can break down the sugars and the mass of incoming carbohydrates is being fermented to short chain fatty acids (SCFAs), mainly acetate, propionate and butyrate. Besides, other metabolites like pyruvate, lactate, succinate and ethanol as well as gases H2, CO2, H2S and CH4 are produced (Whelan, Judd, & Preedy, 2005).

SCFAs are captured by the colonic mucosa and contribute towards energy needs of the host. Acetate is primarily metabolized in the kidney, heart, brain and human muscles, whilst propionate, a glucogenic precursor, suppresses cholesterol production. Butyrate is utilized by the colonic epithelium where it helps in cell growth regulation and differentiation (Sangwan, Tomar, Singh, Singh, & Ali, 2011).

Prebiotics exhibit imperative technological properties as well as attractive nutritional value. In food formulations, they appreciably upgrade sensory features and improve taste and mouth feel. In order to become part of functional food, prebiotics must be stable to processing conditions like heat, pH and Maillard reaction because degraded mono- and disaccharides are not available for bacterial fermentation. Previous investigations on prebiotics have shown that heating at low pH causes reduction in prebiotic activity whilst other conditions did not alter stability (Al-Sheraji et al, 2013, Bohm et al, 2006).

Inclusion of prebiotics in food is a natural way to provide healthy ingredients to the consumers. Most of the prebiotics are easily consumable and give desired functionality to the food items (Courtin, Swennen, Verjans, & Delcour, 2009). For instance, short chain prebiotics act like sugars and contribute to crispiness and browning of the end product. Long chain prebiotics work as fat replacer, escalate the texture and mouthfeel. The majority of the prebiotics are not considerably distorted or damaged by processing treatments, thus retaining their functionality throughout the alimentary tract. Contrarily, most of the probiotics in the finished products have been killed due to harsh processing conditions that are required to eradicate microbes for food safety reasons (Bohm et al., 2006).

Section snippets

Prebiotics and metabolic syndromes

Recent advances to curtail disease progression have opened new avenues for the development of prebiotic-based dietary interventions to halt the incidence of metabolic dysfunction (Riccioni et al., 2012). In the present scenario, production of designer foods with natural ingredients like prebiotics is a pragmatic approach. A number of epidemiological studies have illuminated the cardioprotective effect of diets high in phytochemicals (vitamins, minerals, antioxidants) and fibres (Ignarro,

Bifidogenic effects of prebiotics

Dietary patterns based on therapeutic ingredients influence consumers health in multifarious ways. Likewise, the intestinal probiotics affects numerous physiological aspects and are helpful to generate desirable constituents. The association between colonic microorganisms and vulnerability to diseases has set forth the demand of new functional products for healthy intestinal activity (Peng et al, 2015, Sonnenburg et al, 2010). Diet can alter the functional metabolism of the intestinal

Hypocholesterolaemic perspectives

Increased serum cholesterol and triacylglycerols (TAG) along with (abdominal) obesity, insulin resistance and arterial hypertension are components of the metabolic syndrome. Cholesterol is the main cause for the accumulation of fatty deposits in the inner lining of arteries leading to atherosclerosis and onset of heart disease, stroke and other vascular diseases. It is estimated that about 18% of the stroke events and 56% of the heart diseases worldwide are ascribed to high cholesterol level (

Hypoglycaemic facets

The high prevalence of diabetes in the developing world is shifting towards an epidemic. The striking increase in obesity and weight gain are major risk factors contributing to various metabolic complications. The risk of insulin resistance increases with advancing obesity (Deguchi & Miyazaki, 2010). Obesity may lead to an insulin resistant state in the liver, muscle cells and adipose tissue, resulting in distorted function of insulin targeted cells and buildup of macrophages that secrete

Conclusion

Results from these studies support the potential of prebiotics especially fructooligosaccharides against physiological threats including hypercholesterolaemia, hyperglycaemia and intestinal disorders. Prebiotics appear to exert their beneficial effects through various mechanisms. The studies discussed here provide clinical and experimental evidence for supplementation of diet with prebiotics. However, there are only few human studies which support this hypothesis that warrant the need for

References (106)

  • C. Courtin et al.

    Heat and pH stability of prebiotics arabinoxylooligosaccharides, xylooligosaccharides and fructooligosaccharides

    Food Chemistry

    (2009)
  • C.A. Daubioul et al.

    Dietary oligofructose lessens hepatic steatosis, but does not prevent hypertriglyceridemia in obese zucker rats

    Journal of Nutrition

    (2000)
  • S. Genta et al.

    Yacon syrup: Beneficial effects on obesity and insulin resistance in humans

    Clinical Nutrition

    (2009)
  • S. Ghoshal et al.

    Chylomicrons promote intestinal absorption of lipopolysaccharides

    The Journal of Lipid Research

    (2009)
  • G.R. Gibson et al.

    Dietary modulation of the human colonic microbiota: Introducing the concept of prebiotics

    The Journal of Nutrition

    (1995)
  • F. Guarner et al.

    Gut flora in health and disease

    Lancet

    (2003)
  • S. Guida et al.

    Gut microbiota and obesity: Involvement of the adipose tissue

    Journal of Functional Foods

    (2015)
  • S. Hooda et al.

    454 pyrosequencing reveals a shift in fecal microbiota of healthy adult men consuming polydextrose or soluble corn fiber1-3

    Journal of Nutrition

    (2012)
  • C.K. Hsu et al.

    Xylooligosaccharides and fructooligosaccharides affect the intestinal microbiota and precancerous colonic lesion development in rats

    Journal of Nutrition

    (2004)
  • J. Kellogg et al.

    Alaskan seaweeds lower inflammation in RAW 264.7 macrophages and decrease lipid accumulation in 3T3-L1 adipocytes

    Journal of Functional Foods

    (2015)
  • G.B. Kim et al.

    Effect of dietary prebiotic supplementation on the performance, intestinal microflora, and immune response of broilers

    Poultry Sciences

    (2011)
  • M. Kim et al.

    The water-soluble extract of chicory influences serum and liver lipid concentrations, cecal short-chain fatty acid concentrations and feacal lipid excretion in rats

    Journal of Nutrition

    (1998)
  • S.H. Kim et al.

    Supplementation of infant formula with native inulin has a prebiotic effect in formula-fed babies

    Asia Pacific Journal of Clinical Nutrition

    (2007)
  • D. Letexier et al.

    Addition of inulin to a moderately high-carbohydrate diet reduces hepatic lipogenesis and plasma triacylglycerol concentrations in humans

    American Journal of Clinical Nutrition

    (2003)
  • R.J.F. Manders et al.

    Prevalence of daily hyperglycemia in obese type 2 diabetic men compared with that in lean and obese normoglycemic men: Effect of consumption of a sucrose-containing beverage

    Journal of Clinical Nutrition

    (2009)
  • A. Mortensen et al.

    Effect of a long-chained fructan Raftiline HP on blood lipids and spontaneous atherosclerosis in low density receptor knockout mice

    Nutrition Research

    (2002)
  • A.S. Neish

    Microbes in gastrointestinal health and disease

    Gastroenterology

    (2009)
  • PengM. et al.

    Lactobacillus casei and its byproducts alter the virulence factors of foodborne bacterial pathogens

    Journal of Functional Foods

    (2015)
  • T. Piche et al.

    Colonic fermentation influences lower esophageal sphincter function in gastroesophageal reflux disease

    Gastroenterology

    (2003)
  • H. Rehman et al.

    Effects of dietary inulin on the intestinal short chain fatty acids and microbial ecology in broiler chickens as revealed by denaturing gradient gel electrophoresis

    Poultry Sciences

    (2008)
  • F. Respondek et al.

    Shortchain fructooligosaccharides influence insulin sensitivity and gene expression of fat tissue in obese dogs

    Journal of Nutrition

    (2008)
  • M.E. Rodriguez-Cabezas et al.

    The combination of fructooligosaccharides and resistant starch shows prebiotic additive effects in rats

    Clinical Nutrition

    (2010)
  • E.D. Sonnenburg et al.

    Specificity of polysaccharide use in intestinal bacteroides species determines diet-induced microbiota alterations

    Cell

    (2010)
  • J. Styskal et al.

    Oxidative stress and diabetes: What can we learn about insulin resistance from antioxidant mutant mouse models?

    Free Radical Biology & Medicine

    (2012)
  • P.J. Turnbaugh et al.

    Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome

    Cell Host & Microbe

    (2008)
  • S. Velasco et al.

    Effect of inulin supplementation and dietary fat source on performance, blood serum metabolites, liver lipids, abdominal fat deposition, and tissue fatty acid composition in broiler chickens

    Poultry Sciences

    (2010)
  • K. Whelan et al.

    Fructooligosaccharides and fiber partially prevent the alterations in fecal microbiota and short-chain fatty acid concentrations caused by standard enteral formula in healthy humans

    Journal of Nutrition

    (2005)
  • F.A. Alegria et al.

    The health and nutritional virtues of artichokes – From folklore to science. Proc. of 5th IC on Artichoke ED. F.J. Sanz Villar

    Acta Horticulturae

    (2004)
  • E.M. Alissa et al.

    Functional foods and nutraceuticals in the primary prevention of cardiovascular diseases

    Journal of Nutrition and Metabolism

    (2012)
  • G.H. Anderson et al.

    Physiology of food intake regulation: Interaction with dietary components

    Nestlé Nutrition Workshop Series Paediatric Programme

    (2002)
  • B.R. Balcazar-Munoz et al.

    Effect of oral inulin administration on lipid profile and insulin sensitivity in subjects with obesity and dyslipidemia

    Revista Medica de Chile

    (2003)
  • E.L. Berg et al.

    Fructooligosaccharide supplementation in the yearling horse: Effects on fecal pH, microbial content and volatile fatty acid concentrations

    Journal of Animal Sciences

    (2004)
  • A. Bohm et al.

    Heat-induced degradation of inulin

    European Food Research and Technology

    (2006)
  • Y. Bouhnik et al.

    The capacity of short-chain fructo-oligosaccharides to stimulate faecal bifidobacteria: a dose-response relationship study in healthy humans

    Nutrition Journal

    (2006)
  • L.A. Brandt

    Prebiotics enhance gut health

    Prepared Foods

    (2001)
  • F. Brighenti

    Dietary fructans and serum triacylglycerols: A meta-analysis of randomized controlled trials

    Journal of Nutrition

    (2007)
  • P.D. Cani et al.

    Oligofructose promotes satiety in healthy human: A pilot study

    European Journal of Clinical Nutrition

    (2006)
  • P.D. Cani et al.

    Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability

    Gut

    (2009)
  • ChenY.C. et al.

    Effects of chicory fructans on egg cholesterol in commercial laying hen

    International Journal of Poultry Sciences

    (2005)
  • M.J. Claesson et al.

    Gut microbiota com-position correlates with diet and health in the elderly

    Nature

    (2012)
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