Modifications in bacterial groups and short chain fatty acid production in the gut of healthy adult rats after long-term consumption of dietary Maillard reaction products
Graphical abstract
Introduction
The scientific information supporting the importance of dietary habits in the maintenance of health to the extent they can affect the diversity of the intestinal microbiota is increasing every day (De Filippo et al., 2010). There is growing evidence that bacteria within the colon play an important role in equilibrium of the organism, providing energy for the host, educating the immune system, participating in key physiological-biochemical processes and maybe being implicated in colon cancer pathogenesis (Flint, 2012, Nicholson et al., 2012, Tuohy et al., 2006). Furthermore, the colonic microbiota extracts energy from dietary compounds, which escape digestion in the stomach and small intestine, as well as endogenous substrates such as mucins, secreted by the host. For that reason, the human colonic microbiota must be considered as an anaerobic digester, which acts mainly on material recalcitrant to digestion in the upper gut by using an array of anaerobic metabolic pathways (Nicholson, Holmes, & Wilson, 2005).
The value of foodstuffs is usually linked to their ability to provide energy and nutrients. In developed countries most of the foods consumed are submitted to industrial or domestic processing, which commonly includes thermal treatment. Heating food matrixes rich in proteins, carbohydrates and/or lipids leads to the appearance of the so-called Maillard reaction products (MRPs), a large number of compounds with different chemical structures and molecular weights (Morales, 2005). Among the products formed during the intermediate and advanced stages of the reaction, 5-Hydroxymethylfurfural and the advanced glycation end-product (AGE) carboxymethyl-lysine (CML) have to be mentioned due to their involvement in different physio-phatological processes (Delgado-Andrade, 2016, Pastoriza et al., 2017). On the other hand, during the final stages of the Maillard reaction, polymerization and dehydration mechanisms take place, resulting in nitrogen-containing brown-colored compounds called melanoidins (Cammerer, Jalyschko, & Kroh, 2002), whose main chemical characteristics and high molecular weights depend on both the source of reactants and the reaction conditions (Delgado-Andrade & Morales, 2005). Melanoidins are present in widely consumed dietary components such as coffee, cocoa, bread, malt or honey (Fogliano and Morales, 2011, Pastoriza and Rufián-Henares, 2014). Some investigations highlight the role of melanoidins in vivo since they are able to escape digestion and pass through the upper gastrointestinal tract (Faist and Erbersdobler, 2001, Rufián-Henares and Morales, 2007) reaching the hindgut where it is known for a long time that they can interact with the different microbial species there present (Finot & Magnenat, 1981). Most studies focused on the effect of MRPs on gut microorganisms have been done in vitro by cultivating fecal bacteria in anaerobic fermenters. Thus, Borrelli and Fogliano (2005) showed that BC melanoidins could be metabolized/fermented by the human gut microbiota, and that these specific compounds selectively enhanced the growth of Bifidobacteria, which are considered as desirable due to their health-promoting properties. The same was observed by Jiménez-Zamora, Pastoriza, and Rufián-Henares (2015) with coffee melanoidins. However, in vivo studies in animal models or even dietary intervention trials in healthy human subjects are scarce. As a combination of both types of assays, the study by Seiquer, Rubio, Peinado, Delgado-Andrade, and Navarro (2014) must be mentioned. This previous investigation showed that dietary MRPs were able to modulate in vivo the intestinal microbiota composition both in humans and in rats, and that the specific effects are likely to be linked to the chemical structure and the dietary amounts of the different browning compounds. However, model MRPs (i.e. laboratory produced glucose-lysine derivatives), quite different from bread crust MRPs, were used in this earlier work. Also, we were unable to establish what products were potentially responsible for the observed effects, since a pool of all MRPs formed was used in the diets.
Accordingly, the goal of the present work was to analyze the impact of consuming diets containing defined amounts of MRPs from BC, one of the major sources of these compounds in the Western diet, on some interesting bacterial species of the gut microbiota of adult rats. The production of SCFAs derived from the gut microbiota metabolism was also investigated. Additionally, in order to understand MRPs degradation by the gut microorganisms, the molecular masses of the different compounds appearing in feces was investigated. Special attention was paid to the insoluble and soluble high and low molecular weight compounds present in BC, which were isolated and studied separately in order to identify the type of compounds potentially responsible for the observed effects.
Section snippets
Chemicals
All chemicals used were of analytical grade and were obtained from Merck (Darmstadt, Germany), unless stated otherwise. Pronase E (4,000,000 PU/g) was also purchased from this same company. HPLC-grade chemicals were obtained from Lab-San (Dublin, Ireland).
Preparation of diets
The AIN-93G purified diet for laboratory rodents (Dyets Inc., Bethlehem, PA) was used as the control diet. BC was supplied by a Spanish manufacturer of cereal-derived food products. The process by which the BC was cleaned of crumb, and the
Intake of MRPs markers
The daily intake of different MRPs from the dietary treatments is depicted in Table 1. Food consumption was previously published and was as follows: 14.2 ± 0.5, 14.1 ± 0.3, 13.9 ± 0.3, 13.6 ± 0.3 and 12.9 ± 0.4 g/day for the Control, BC, LMW, HMW and Insoluble groups, respectively (Roncero-Ramos, Delgado-Andrade, Haro, Ruiz-Roca, Morales & Navarro, 2013). It is noteworthy that the consumption of the Control diet (AIN-93G) already involved the ingestion of certain basal amounts of these compounds. Their
Acknowledgement
This research was supported by the Spanish Ministry of Science and Innovation under the project AGL2010-15235 and the postdoctoral scholarship of S. Pastoriza from Instituto Danone (Spain). The work has been also partially supported by the FEDER and FSE funds from the European Union.
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2021, Journal of Cleaner ProductionCitation Excerpt :Other studies that have demonstrated the chelating capacity of SCG, by using this food by-product to decontaminate polluted water with heavy metals (Mohamed and Yee, 2019). The chelating capacity of coffee melanoidins could be attributed to their anionic charge (Rufián-Henares and de la Cueva, 2009), which is also the responsible for their antimicrobial activity (Rufián-Henares and Morales, 2008; Delgado-Andrade et al., 2017). Similarly, Wen et al., 2004, Takenaka et al. (2005) also described a polymer extracted from coffee brew (possibly melanoidins), with metal chelating properties against Fe, Zn and Cu.