Nutrition. 2015 Apr 32(4):491-497
Soluble arabinoxylan enhances large intestinal microbial health biomarkers in pigs fed a red meat-containing diet.
Williams BA1, Zhang D1,2, Lisle AT2, Mikkelsen D1, McSweeney CS3, Kang S3, Bryden WL1,2, Gidley MJ1
1 The University of Queensland, Australian Research Council Centre of Excellence in Plant CellWalls, QAAFI Centre for Nutrition and Food Sciences, St. Lucia Campus, Queensland, Australia
2 The University of Queensland, School of Agriculture and Food Sciences, Gatton, Queensland, Australia
3 CSIRO Agriculture Flagship, St. Lucia, Queensland, Australia
To investigate how moderately increased dietary red meat combined with a soluble fibre (wheat arabinoxylan-AX) alters the large intestinal microbiota, in terms of fermentative end-products, and microbial community profiles, in pigs.
Four groups of ten pigs were fed Western-type diets containing two amounts of red meat, with or without a solubilized wheat arabinoxylan-rich fraction for four weeks. Following euthanasia, fermentative end-products (short-chain fatty acids (SCFA), ammonia) of digesta from four sections of large intestine were measured. Di-amino-pimelic acid (DAPA) was a measure of total microbial biomass, and bacterial profiles were determined using a phylogenetic microarray. A factorial model determined effects of AX and meat content.
Arabinoxylan was highly fermentable in the caecum, as indicated by increased SCFA
(particularly propionate) concentrations. There were also decreased protein fermentation end-products, as indicated by the reduced ammonia, and branched-chain ratio, though this effect was less prominent distally. Microbial profiles in the distal large intestine differed in the presence of AX (including promotion of Faecalibacterium prausnitzii), consistent with an increase in carbohydrate versus protein fermentation. Increased DAPA (P<0.0001) suggested increased microbial biomass for animals fed AX.
Solubilised wheat AX has the potential to counteract the effects of dietary red meat, by reducing protein fermentation with its resultant toxic end-products such as ammonia, as well as leading to a positive shift in fermentation end-products and microbial profiles in the large intestine.
Long-term consumption of higher-protein diets is likely to predispose individuals to a range of diseases, due to the production of toxic metabolites from protein fermentation. In particular, consumption of red and processed meats has been associated with increased risk of colo-rectal cancer (Cross et al, 2010). This deleterious effect has been shown to be counteracted by the addition of carbohydrate, such as resistant starch (Toden et al, 2005).
Arabinoxylan is a major soluble fibre component of endosperm cell walls in wheat grains. While usually present in comparatively low amounts (~3% of the whole grain), given the popularity of wheat consumption, it may be one of the most ingested soluble fibres in the Western diet.
We wanted to know whether potentiall negative effects of a modest increase in meat consumption could be offset by the presence of arabinoxylan (AX) in terms of various gut health biomarkers. Our hypothesis was that fermentation of AX in the large intestine of pigs would alter the balance of metabolites from a more protein-based fermentation to one of more carbohydrate-based fermentation. If this were the case, we would detect increased short-chain fatty acids, reduced potentially harmful metabolites such as ammonia, and a positive modification of the microbial population. All of these biomarkers have been related to a decreased risk of colo-rectal cancer.
We fed four different diets to pigs which are considered to be a good model for humans, particularly for their digestive tract physiology and, more recently, their gut microbiology. The four diets, which were nutritionally balanced for pig health, had lower and higher amounts of barbequed red meat, with and without added AX (~ 8%).
Overall, the addition of AX to the diet led to positive differences in almost all parameters examined after 4 weeks. End-products of carbohydrate-based fermentation were increased, while those for protein were decreased. In addition, the presence of AX was associated with both an increased digesta moisture content in all LI sections, and an increased apparent amount of actual bacteria (as indicated by di-amino pimileic acid) (Zhang et al, 2015).
In terms of the microbial populations, for the AX-fed pigs, Faecalibacterium prausnitzii and Bifidobacterium sp. were present in greater abundance (both associated with gut health), while potentially negative species such as Clostridium perfringens was greater in the non-AX-fed pigs.
The benefits of AX reported here relate to both the nature and amount of microbial fermentation metabolites and to changes in the relative abundances of microbial species. Dietary AX also led to compositional changes in digesta that can be directly related to carbohydrate versus protein fermentation in the large intestine, where fermentation started immediately at the cecum.
While past research suggests that insoluble fibre is more protective against colorectal cancer than soluble fibres, we would argue that the solubility per se does not confer protection, but rather fermentability in terms of kinetics and end-products, is more important in determining the health benefits of a particular carbohydrate in the large intestine.
This study provides strong evidence that solubilized AX originating from wheat is an effective ingredient for stimulating carbohydrate fermentation in the large intestine, thereby lowering protein fermentation, at least in part, by providing the metabolic energy for microbial growth and division that provides a sink for residual dietary protein.
Boleij A, Tjalsma H (2012) Gut bacteria in health and disease: a survey on the interface between intestinal microbiology and colorectal cancer. Biological Reviews 87:701-730
Cross AJ, Ferrucci LM, Risch A, Graubard BI, Ward MH, Park Y, Hollenbeck AR, Schatzkin A, Sinha R (2010) A large prospective study of meat consumption and colorectal cancer risk: an investigation of potential mechanisms underlying this association. Cancer Res 70:2406
Toden S, Bird AR, Topping DL, Conlon MA (2005) Resistant starch attenuates colonic DNA damage induced by higher dietary protein in rats. Nutrition & Cancer 51:45-51
Zhang D, Williams BA, Mikkelsen D, Li X, Keates HL, Lisle AT, Collins HM, Fincher GB, Bird AR, Topping DL, Gidley MJ, Bryden WL (2015) Soluble arabinoxylan alters digesta flow and protein digestion of red meat-containing diets in pigs. Nutrition 31: 1141-1147