Particle size of dietary fibre has diverse effects on in vitro gut fermentation rate and end-products depending on food source
Graphical abstract
Introduction
Some carbohydrate polymers and associated components, termed dietary fibre (DF), which escape digestion and absorption in the human small intestine, reach the large intestine where they can be fermented by host microbiota (Jones, 2014). The fermentation of DF by large intestinal microbes produces short-chain fatty acids (SCFA), mainly acetate, propionate and butyrate, via different pathways (Esquivel-Elizondo, Ilhan, Garcia-Peña, & Krajmalnik-Brown, 2017; Koh, De Vadder, Kovatcheva-Datchary, & Bäckhed, 2016; Louis & Flint, 2017). SCFA had been found to exert physiological benefits such as inhibiting the development of some cancers, reducing inflammation, and stimulating immune homeostasis (Koh et al., 2016). Gases are also produced during DF fermentation, potentially causing undesirable effects such as excessive flatulence and abdominal symptoms (Manichanh et al., 2014). To estimate where and how various DF are fermented, determining the in vitro rate and extent of DF fermentation is gaining interest. Little or no DF in the diet, or only poorly fermentable dietary DF could lead to only minor release of SCFA along the large intestine, which has been associated with a higher risk of colorectal cancer (Shuwen et al., 2019). In contrast, rapidly fermentable DF could cause excessive gas production in the proximal colon and consequently less fermentation and SCFA release at the distal colon.
To investigate the fermentation extents and rates, many studies have focused on purified and/or simple DF such as inulin, fructo-oligosaccharides, pectins, or resistant starches, rather than complex DF from plant-based foods (Wang et al., 2019). In the past, one form of DF classification was based on its solubility (McCleary et al., 2012). However, the categorisation of DF based on solubility is considered to only weakly relate to the physiochemical properties of DF and its nutritional functionalities (Gidley & Yakubov, 2019). Also, soluble and insoluble DF could have comparable fermentation extents and rates. For example, soluble and insoluble DF from wheat, rye and barley flours were found to be comparable in terms of gas kinetics and SCFA production (Comino, Williams, & Gidley, 2018). Fermentation of insoluble food particles by microbes could be determined by both substrate surface characteristics (as influenced by particle size) as well as chemical composition, which is normally the major factor in soluble DF fermentation (Day, Gomez, Øiseth, Gidley, & Williams, 2012; Low, Williams, D'Arcy, Flanagan, & Gidley, 2015a; Stewart & Slavin, 2009). Particle size reduction of plant-based foods, caused by food processing and oral mastication, is an important factor that relates substrate surface characteristics (e.g. larger surface area) and the chemical fractions (e.g. total DF and starch content) (Low et al., 2015a; Stewart & Slavin, 2009; Thakkar, Tuncil, Hamaker, & Lindemann, 2020). However, the relative importance of particle size and chemical composition in determining DF fermentation extents, rates and end-products is not understood.
In this study, a wide range of food and ingredients, including sorghum (Sgh) and wheat grains (Wht), almond (Almd), chickpea (Chkp), apple (App), carrot (Crt), wheat bran (WBr) and oat bran (OBr), were fractionated into diverse particle sizes. These food particles were washed and/or digested prior to in vitro fermentation with a pooled human faecal inoculum. Gas production was recorded in time, and the final SCFA and ammonia concentrations analysed, to assess the fermentation end-products and rates for each food and particle size. We hypothesized that: i) the fermentation end-products and rates for the same food/ingredient with different particle sizes will vary; ii) between food types, particle size will have different effects on fermentation rates and extents; and iii) a combination of chemical composition and particle size will determine DF fermentation outcomes.
Section snippets
Substrate preparation
Food particles (i.e., Sgh, Wht, Almd, Chkp, App, Crt, WBr, OBr) were prepared from ingredients purchased from a local supermarket in Brisbane, Australia. The maize starch (MStch) was sourced from Penford Australia Ltd (Lane Cove, Australia). Almonds had been pre-blanched by the manufacturer. Apple and carrot were peeled, and the flesh was collected. All the particles were blended to reduce the particle size, followed by passing through a set of sieves to obtain particles of defined size ranges.
Substrate characteristics
Many food processing methods reduce particle size, even the simple process of chewing breaks down food structure and can rupture structural features such as cells. The effect of food particle size reduction depends on the homogeneity of the food and how the internal contents are released. Sorghum showed a compact structure for different particle sizes, and these samples had a high starch content for all particles sizes (Fig. 1, Table 1), indicating that starch is not necessarily released after
Conclusions
In summary, this study has investigated the effect of particle size on the in vitro fermentation of a broad range of food particles (from grains, legumes, nuts, vegetables, fruits and brans). However, particle size differences in the range of 60 μm to 4 mm result in marked differences in chemical composition for the same food source, primarily due to a greater number of intact cells with entrapped components at larger particle sizes. By combining the major chemical composition analysis and
CRediT authorship contribution statement
Hong Yao: Conceptualization, Investigation, Writing – original draft. Bernadine M. Flanagan: Methodology, Investigation, Writing – review & editing. Barbara A. Williams: Methodology, Formal analysis, Investigation, Writing – review & editing. Deirdre Mikkelsen: Methodology, Investigation, Writing – review & editing. Michael J. Gidley: Conceptualization, Supervision, Writing – review & editing.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgement
The authors acknowledge financial support for a scholarship to HY from the China Scholarship Council and the University of Queensland. The authors would like to thank the following colleagues for their invaluable assistance during the in vitro experiment: Alex Bui, Shiyi Lu, Widaningrum, Romane Dusfour-Castan, and Meaghan Rochoy. SCFA analysis was conducted by Mr. Peter Isherwood (University of Queensland, Gatton campus), and the ammonia analysis by Mr. Brian Burren at DAF (Cooper's Plains,
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