Dietary fibre: Relating functionality to molecular structure

Dietary fibres confer numerous benefits as part of a healthy diet, but these are specific to which fibres are consumed.

Dietary fibres are indigestible carbohydrates that confer many potential health benefits, including risk reductions for several chronic diseases, but both molecular and intermolecular, longer-scale structures and hence physical properties of indigestible carbohydrates can vary widely. As a result, to understand the physiological functionality of individual dietary fibre sources inside the gastro-intestinal tract and the mechanisms by which they affect these diseases, we need to re-examine molecular/microscopic structure-physical function relationships.

Understanding this connection between health benefits and physical structures and properties of dietary fibre has been a theme of both of our research groups for many years. We will discuss this link with a focus on glycemia control. We will also demonstrate the importance of health messaging specific to the type of fibre, rather than broad classifications.

Dietary fibre and health

Dietary fibre in the diet has been associated for many years with numerous health benefits, including glycemia control and risk reduction of Type II diabetes; cholesterol lowering and risk reduction of coronary vascular and heart disease; enhanced satiety for weight management and risk reduction of obesity; risk reduction of gastroesophageal reflux disease; risk reduction of diverticulosis and colorectal cancers; and enhanced colon health by acting as a prebiotic to support the growth of beneficial bacteria.1-3 Most of these effects can be related to specific properties of the individual fibres when in the conditions found within the stomach or the small intestine, as shown by previous work of others and which we will discuss in more detail based on our own work.4-6

Understanding the chemistry and structure of dietary fibre

Polysaccharides are carbohydrates that contain at least ten monosaccharide sugar residues, in most cases 1000s, linked together with glycosidic bonds. In food and nutrition, they can be classified as starch or non-starch polysaccharides, the main difference being that starch is digested by human enzymes to produce glucose, which is absorbed and utilised (hence referred to as glycemic), whereas non-starch polysaccharides are indigestible by human digestive enzymes (hence non-glycemic). The non-starch polysaccharides are the major source of dietary fibres. Within this group, there is a a vast array of chemical structures and physical behaviours, depending on their food source. Examples include plant structural polysaccharides such as cellulose and the hemicelluloses (e.g. arabinoxylans, β-glucans or pectin); seed or tuber storage polysaccharides (e.g. guar gum, locust bean gum or psyllium); plant exudates such as gum Arabic; seaweed polysaccharides (such as alginates or carrageenan’s); and bacterial polysaccharides (e.g. dextran, gellan or xanthan gums). All these differ according to the types of sugar residues present (including arabinose, xylose, glucose, galactose and mannose, and the uronic acid forms of these sugars), the molecular weight (which can range from ten thousand to the millions), and their physical structure. They can be long, linear, stiff chains, such as cellulose or xanthan gum, or they can be linear flexible chains such as carrageenans or alginates. They can also be singly substituted, such as guar or locust bean gum (galactomannans), or highly branched, such as pectin, gum Arabic or dextran.

Many of these non-starch polysaccharides are used as food ingredients for thickening, emulsion and foam stability, and gelation. Applications are diverse; from jams and jellies, to sauces and salad dressings, and from batters for fried foods, to sausages and meat products. There exists a great deal of knowledge about the relationships between molecular structure and physical functionality in the context of these food applications, based largely on their intramolecular volume and intermolecular interactions. Intramolecular volume depends on molecular weight and on molecular structure – bond angles, chain stiffness, degree of branching, etc. Intermolecular interactions depend on the ability of molecules to align and cross-bond to form three-dimensional space-filling networks. Their viscosity and gelation profiles have been extensively studied by rheology and numerous other techniques and can be predicted based on physical structure. It should be possible to extend this knowledge to their behaviour within the stomach, small intestine and large intestine, at the appropriate pH and concentration and with other food molecules at the various stages of the digestion system.

In contrast with the extensive knowledge of physical properties for refined polysaccharides used in food structuring, less is known about the behaviour of non-refined polysaccharides as found in the cell walls of plants. These natural polysaccharide networks are the basis for the physical structure of health-associated food components including wholegrain cereals, fruits, vegetables, legumes and nuts. Depending on the molecular composition of cell walls from these diverse foods, they can exhibit extensive swelling (such as oat porridge and tomato paste) or retain dense non-swelling characteristics (e.g. nuts and corn kernels). Here, both the molecular composition and the natural architecture of the cell wall material influence the physical properties and their behaviour under conditions found in the digestive tract.

Dietary fibre and glycemia control

One of the many biological functionalities of dietary fibre when present in the human diet is its ability to reduce the rate of absorption of glucose after consumption of glycemic carbohydrate-containing foods, leading to a blunted blood glucose response curve and less demand for insulin. Glycemia (post-prandial blood glucose concentration) control through dietary intervention is very important for those with mild Insulin Resistance through to those with Type II Diabetes Mellitus, a population that is growing globally at an alarming rate. A recently published meta-analyses of 617,968 participants and 41,066 incident cases of Type II diabetes showed that relative risk was reduced to 0.75 with 10 g/day increase in cereal fibre intake.7 This is a very remarkable result, corroborating many earlier clinical trials.1

Diverse dietary fibre effects in the digestive tract can be rationalised based on their ability to structure digesta, bind to food and digestive tract components, and influence the transport of nutrients and digestive enzymes. When the physiology of starch and sugar digestion and glucose absorption is considered, it is possible to elucidate several plausible mechanisms by which the dietary fibres might contribute to glycemia control: reduction in gastric emptying, inhibition of amylase activity and delayed starch hydrolysis, reduction in diffusion of amylolytic products to the small intestinal microvilli, and/or the development of an absorptive barrier layer through interactions with the mucosa.8 Our results indicate that all of the mechanisms above are involved to some extent. Delayed starch hydrolysis can clearly be demonstrated in vitro but our in vivo results suggest that gastric emptying and/or mucosal interactions are also significant to fibre functionality in glycemia control, as discussed in more detail below.

Relating the physical and physiological functionality of dietary fibre

In a series of projects in the Goff laboratory, isolated non-starch polysaccharides of widely varying molecular structures were compared at various concentrations for their ability to delay starch hydrolysis. All the experimental polysaccharides delayed hydrolysis to some extent, but not dependent on concentration. The rheological behaviour of the polysaccharide and starch solutions was studied in simulated digestion experiments, mimicking gastric and small intestinal conditions. Some of the polysaccharides were better able to retain their viscosity through the simulated digestion than others, and this was dependent on their intramolecular structures and intermolecular interactions.

Correlations were seen between viscosity in the small intestinal conditions and starch hydrolysis rates. We took this information and designed a human clinical trial in which we formulated a pudding-like product containing either starch or maltose as the available carbohydrate and with several dietary fibres and controls.9 Gastric emptying rate was measured along with blood glucose and insulin two-hour response. The products were formulated to match their predicted small intestinal viscosity after digestion, and this resulted in widely different concentrations of polysaccharides being used, because of the range of molecular structures that were chosen. We found that blood glucose and insulin were blunted in dietary fibre-containing products compared to controls, and that the blood glucose levels were similar amongst fibre-containing products despite the widely differing concentrations. Thus, it appears that when matched for simulated small intestinal viscosity, gums of widely varying molecular structure, and hence concentration, behave similarly with respect to glycemia control.

We also demonstrated that gastric emptying rates were delayed due to the intermolecular associations of the polysaccharides within the gastric environment. Although there were significant differences between the starch and maltose containing products, suggesting the contribution of enzyme activity, the products containing maltose and fibres also led to lower blood glucose levels relative to control, suggesting also an important role for gastric behaviour of the dietary fibres in slowing down gastric emptying. From these results, we have shown that rheological behaviour of dietary fibre, as predicated by molecular structure, can be used to predict both gastric emptying and starch hydrolysis within the conditions of both of those environments. Dietary fibre functionality for glycemia control is not a direct function of either concentration or product viscosity, but rather rheological behaviour within the both stomach and small intestinal conditions, as determined by molecular structure.

It is possible to connect the use of isolated fibres for glycemia control, as discussed above, with the properties of plant tissue foods such as wholegrains, fruits and vegetables that form the majority of fibre intake in most human diets. It has been common to classify non-starch polysaccharides/dietary fibres as soluble or insoluble, with properties such as viscosity and gelling ability in the stomach and small intestine, and fermentability by colonic bacteria conventionally associated with soluble fibres, and control of digesta transport and faecal passage associated with insoluble fibre. Recent work in the Gidley laboratory has illustrated how this is an inadequate division of properties, resulting in the proposal that a combination of (molecular or particle) size and local density of packing of polysaccharides is required to explain the diverse and overlapping property sets associated with the wide range of food materials classified as dietary fibre.10,11

One characteristic of plant-based foods is the encapsulation ability of plant cell walls, with consequences on the glycemic response to starchy foods such as legumes and cereals. Indeed, for a range of legumes, a single intact cell wall is sufficient to prevent starch-degrading enzymes from accessing the starch encapsulated within cells.12 This provides an example of dietary fibre action based on both binding (enzymes bind with the polysaccharides within plant cell walls, particularly cellulose) and transport (cell walls as a physical barrier to passage of enzymes), which complements the digesta structuring effects of added soluble fibres. The retention of plant cellular structure has been shown to be a viable approach to control of glycemia in vivo, through the demonstration of blunted insulin and blood glucose responses to wheat-based foods containing particles greater than 2mm in size compared with traditional flour.13 This demonstration of highly effective glycemic control through particle size effects alone provides a good example of the need to take into account physical as well as molecular structures contributing to dietary fibre properties in the digestive tract.

A further potential site of action for both isolated and plant-based dietary fibres is the mucus layer that covers the surface of the digestive tract and helps to control access of digested nutrients to the epithelial cells and subsequent entry into the blood stream. Both isolated polysaccharides and plant cell wall materials have been shown to interact with mucin gels in vitro, with an interesting difference in interaction mechanism between negatively charged polysaccharides such as pectin (binding to the positively charged components in mucin) and neutral polysaccharides such as cereal arabinoxylan and β-glucan (interpenetration of polymers into the mucin network).14 It is not yet clear whether mucus-level interactions can contribute to glycemic control, but it seems likely by analogy with the interactions between oat β-glucan and the mucus layer, associated with reduction in blood cholesterol levels.15 In addition to the roles of gastric and small intestinal environments, some of the effects of dietary fibres on glycemia control may also be mediated by microorganisms, particularly in the colon. Although direct effects of dietary fibres on blood glucose levels are due to gastric and small intestinal factors, fermentation of dietary fibres by gut microbiota generates hormonal signals that can play a role in body management of glycemic dietary components. As gut microbiota science continues to develop, we should expect further refinement in understanding of its role in glycemic control, as modulated by dietary fibres.

Dietary fibre and health claims

Understanding the relationships between molecular structure, physical functionality and physiological functionality should enable the food industry to deliver more fibre-enriched functional food products to consumers, which satisfy both food quality and nutritional value. It is clear, however, that claims regarding dose-response relationships need to be specific both to the type of fibre and the physiological response outcome. This is exemplified by the European Food Safety Authority health claim for β-glucan and post-prandial glycemic response (4g β-glucan for each 30g available carbohydrate). We propose that such dose-response relationships for non-starch polysaccharides should become more predictable by enhanced consideration of molecular structure – physical functionality relationships.

References

 

1          J.W Anderson et al. 2009. it Health benefits of dietary fiber. Nutrition Reviews 67: 188–205

2          I.A Brownlee. 2011. The physiological roles of dietary fibre. Food Hydrocolloids 25: 238–250

3          M.J Gidley. 2013. Hydrocolloids in the digestive tract and related health implications. Current Opinion in Colloid & Interface Science 18: 371–378

4          A.J Wanders et al. 2011. Effects of dietary fibre on subjective appetite, energy intake and body weight: a systematic review of randomized controlled trials. Obesity Reviews 12: 724-739

5          P.I Chater et al. 2015. The impact of dietary fibres on the physiological processes governing small intestinal digestive processes. Bioactive Carbohydrates and Dietary Fibre 6: 117–132

6          A. Mackie, B. Bajka, and N. Rigby. 2016. Roles for dietary fibre in the upper GI tract: The importance of viscosity. Food Research International 88: 234–238

7          The InterAct Consortium. 2015. Dietary fibre and incidence of type 2 diabetes in eight European countries: the EPIC-InterAct Study and a meta-analysis of prospective studies. Diabetologia 58: 1394–1408

8          H.D Goff et al. 2018. Dietary fibre for glycemia control: towards a mechanistic understanding. Bioactive Carbohydrates and Dietary Fibre 14: 39-53.

9          B.A Kay et al. 2017. Pudding products enriched with yellow mustard mucilage, fenugreek gum or flaxseed mucilage and matched for simulated intestinal viscosity significantly reduce postprandial peak glucose and insulin in adults at risk for type 2 diabetes. J. Functional Foods. 37:603-611

10        M.L Grundy et al. 2016. Re-evaluation of the mechanisms of dietary fibre and implications for macronutrient bioaccessibility, digestion and postprandial metabolism. British Journal of Nutrition 116: 816-823

11        M.J Gidley and G.E Yakubov. 2019. Functional categorisation of dietary fibre in foods: Beyond ‘soluble’ vs ‘insoluble’. Trends Food Sci Technol 86: 563–568

12        S. Dhital et al. 2016. Intactness of cell wall structure controls the in vitro digestion of starch in legumes. Food & Function 7: 1367–1379

13        C.H Edwards et al. 2015. Manipulation of starch bioaccessibility in wheat endosperm to regulate starch digestion, postprandial glycemia, insulinemia, and gut hormone responses: A randomized controlled trial in healthy ileostomy participants. Amer J Clinical Nutrition 102: 791-800

14        O. Meldrum et al. 2017. Mucoadhesive functionality of cell wall structures from fruits and grains: Electrostatic and polymer network interactions mediated by soluble dietary polysaccharides. Scientific Reports 7: 15794

15        N. Gunness et al. 2016. Reduction in circulating bile acid and restricted diffusion across the intestinal epithelium are associated with a decrease in blood cholesterol in the presence of oat β-glucan. FASEB Journal 30: 4227-4238

 

Prof H Douglas Goff

University of Guelph

Prof Michael J Gidley

The University of Queensland

dgoff@uoguelph.ca

m.gidley@uq.edu.au

https://www.uoguelph.ca/foodscience/

https://qaafi.uq.edu.au/centre-for-nutrition-and-food-sciences

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