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

https://doi.org/10.1016/j.foodres.2017.06.067Get rights and content

Highlights

  • MRPs from bread crust affect gut microbiota composition and SCFAs production.

  • Lactobacilli and Bifidobacteria decreased, while Escherichia/Shigella group increased.

  • Consumption of bread crust induced a high production of formic and propionic acids.

  • Fecal excretion of isolated compounds reflected the products ingested in the diets.

Abstract

Bread crust (BC) is one of the major sources of Maillard reaction products (MRPs) in the Western diet. This work was designed to analyze the impact of diets containing important levels of MRPs from BC on intestinal bacterial growth and short chain fatty acids (SCFAs) production in adult rats. Additionally, the pools of compounds excreted in feces attending to their molecular weights were analyzed. Rats were fed for 88 days a control diet or diets containing BC or its soluble high molecular weight (HMW), soluble low molecular weight (LMW) or insoluble fractions, respectively. Intestinal (cecum) microbiota composition was determined by qPCR analysis. Consumption of the BC diet lowered (P < 0.05) Lactobacillus spp. and Bifidobacterium spp. log10 counts (8 and 14%, respectively), an effect for which soluble LMW and HMW fractions of BC seemed to be responsible. In these same animals, Escherichia/Shigella counts increased by around 45% (P < 0.05), a fact which correlated with a higher production of formic acid in feces (r = 0.8197, P = 0.0458), and likely caused by the combined consumption of all MRPs contained in the BC. A significant 5-fold increment (P < 0.05) was detected in the fecal proportion of propionic acid in the BC group, one of the products that have largely been associated with anti-inflammatory actions. Regarding the distribution of MRPs in feces, only the LMW fed group exhibited a predominance of those ranging between 90,000–1000 Da, whereas the rest of the groups presented higher amounts of products above 90,000 Da. It is concluded that dietary Maillard reaction products are in vivo fermented by the gut microbiota, thereby changing both the pattern of SCFAs production and the microbiota composition.

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.

References (57)

  • M.J. Peinado et al.

    Effects of inulin and di-d-fructose dianhydride-enriched caramels on intestinal microbiota composition and performance of broiler chickens

    Animal

    (2013)
  • W. Scheppach et al.

    Role of short-chain fatty acids in the prevention of colorectal cancer

    European Journal of Cancer

    (1995)
  • S.Y. Tang et al.

    Non-enzymatic glycation alters microdamage formation in human cancellous bone

    Bone

    (2010)
  • J.M. Ames et al.

    The effect of a model melanoidin mixture on fecal bacterial population in vitro

    British Journal of Nutrition

    (1999)
  • M. Asarat et al.

    Extraction and purification of short-chain fatty acids from fermented reconstituted skim milk supplemented with inulin

    Food Analytical Methods

    (2016)
  • R.C. Borrelli et al.

    Characterization of a new potential functional ingredient: Coffee silverskin

    Journal of Agricultural and Food Chemistry

    (2004)
  • R.C. Borrelli et al.

    Bread crust melanoidins as potential prebiotic ingredients

    Molecular Nutrition & Food Research

    (2005)
  • B. Cammerer et al.

    Carbohydrate structures as part of the melanoidin skeleton

    Journal of Agricultural and Food Chemistry

    (2002)
  • A. Costabile et al.

    Whole-grain wheat breakfast cereal has a prebiotic effect on the human gut microbiota: A double-blind, placebo-controlled, crossover study

    British Journal of Nutrition

    (2008)
  • J.H. Cummings

    The large Intestine in Nutrition and Disease. Danone chair monograph

    (1997)
  • C. De Filippo et al.

    Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa

    Proceedings of the National Academy of Sciences of the United States of America

    (2010)
  • C. Delgado-Andrade et al.

    2012. Study of the urinary and faecal excretion of Ne-carboxymethyllysine in young human volunteers

    Amino Acids

    (2012)
  • C. Delgado Andrade et al.

    Effect of diets supplemented with MRPs from bread crust in food intake and body weights in rats

    Food & Function

    (2013)
  • C. Delgado-Andrade

    Carboxymethyl-lysine: Thirty years of investigation in the field of AGE formation

    Food & Function

    (2016)
  • C. Delgado-Andrade et al.

    Unraveling the contribution of melanoidins to the antioxidant activity of coffee brews

    Journal of Agricultural and Food Chemistry

    (2005)
  • C. Dell'Aquila et al.

    Fermentation of heated gluten systems by gut microflora

    European Food Research and Technology

    (2003)
  • V. Faist et al.

    Metabolic transit and in vivo effects of melanoidins and precursors compounds deriving from the Maillard reaction

    Annals of Nutrition & Metabolism

    (2001)
  • P.A. Finot et al.

    Metabolitic transit of early and advanced Maillard products

  • Cited by (59)

    • Role of gut microbiota in food safety

      2022, Present Knowledge in Food Safety: A Risk-Based Approach through the Food Chain
    • Spent coffee grounds as a source of smart biochelates to increase Fe and Zn levels in lettuces

      2021, Journal of Cleaner Production
      Citation 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.

    View all citing articles on Scopus
    View full text