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INTERACTION BETWEEN FOOD PYRAMID AND GUT MICROBIOTA. A NEW NUTRITIONAL APPROACH

Interação entre a pirâmide alimentar e a microbiota intestinal. Uma nova abordagem nutricional

ABSTRACT

The food pyramid is a pre-established nutritional education tool. The integration between the intestinal microbiome, food groups, and SCFA-producing bacteria, which benefit from the ingestion of these foods, has the potential to further improve and innovate healthy eating. The diet-microbiome interaction needs to be incorporated into nutrition science, and the food pyramid might assist in this interaction and nutritional learning. Against this context, this brief communication proposes through the food pyramid, the interactions between the intestinal microbiota, food groups, and SCFAs-producing bacteria.

Keywords:
Microbiota; food pyramid; nutrition

RESUMO

A pirâmide alimentar é uma ferramenta pré-estabelecida de educação nutricional. A integração entre microbioma intestinal, grupos de alimentos e bactérias produtoras de ácidos graxos de cadeia curta (AGCC), que se beneficiam da ingestão de carboidratos fermentáveis, tem o potencial de melhorar e inovar ainda mais a proposta de alimentação saudável. O conceito dieta-microbiota intestinal pode ser incorporado à ciência da nutrição, e a pirâmide alimentar pode auxiliar nessa interação nutricional. Diante desse contexto, esta breve comunicação propõe, por meio da pirâmide alimentar, a ampliação do conhecimento entre a microbiota intestinal, grupos alimentares e bactérias produtoras de AGCC.

Palavras-chave:
Microbiota; pirâmide alimentar; nutrição

HIGHLIGHTS

•Integration between food pyramid and gut microbiome.

•Negative and positive effects of food on the gut microbiome using the food pyramid.

•SCFA-s-producing bacteria and their effects on the gut microbiome.

INTRODUCTION

The food pyramid emerged in the United States in 199211. Welsh S, Shaw A, Davis C. Achieving dietary recommendations: whole-grain foods in the Food Guide Pyramid. Crit Rev Food Sci Nutr. 1994;34:441-51. and was adapted for the Brazilian population by Philippi et al. in the late 1990s22. Tucunduva PS, Romero LA, Rodrigues CAT, Cisotto RL. Adapted food pyramid: a guide for a right food choice. Rev. Nutr. 1999;12:65-80. doi.org/10.1590/S1415-52731999000100006. The food pyramid is used as an instrument for the nutritional guidance of individuals and population groups, respecting their eating habits and the different regional and institutional realities. Its original purpose was to convey two main ideas: variety and proportionality, both by images and by the size of the food group22. Tucunduva PS, Romero LA, Rodrigues CAT, Cisotto RL. Adapted food pyramid: a guide for a right food choice. Rev. Nutr. 1999;12:65-80. doi.org/10.1590/S1415-52731999000100006. However, it is still very focused on nutrients and not on foods.

This food and nutrition education tool has been widely used to emphasize in the population the importance of increasing consumption of grains, vegetables, and fruits, as part of a healthy diet to prevent the development of chronic diseases.

Similarly, the last 15 years have seen unprecedented progress in microbiome research and the first attempts to clinically manipulate the gut microbiota to treat and prevent these diseases33. Jiang Z, Sun TY, He Y, Gou W, Zuo LS, Fu Y, et al. Dietary fruit and vegetable intake, gut microbiota, and type 2 diabetes: results from two large human cohort studies. BMC Med. 2020;18:371..

The role that the microbiota plays in intestinal function and in maintaining the health of the host depends on a balance between potentially pathogenic bacteria and numerous non-pathogenic microorganisms, which are distributed in four major phyla in the human intestine: bacteroidetes and firmicutes which correspond to 90% and proteobacteria and actinobacteria44. Aslam H, Marx W, Rocks T, Loughman A, Chandrasekaran V, Ruusunen A, et al. The effects of dairy and dairy derivatives on the gut microbiota: a systematic literature review. Gut Microbes. 2020;12:1799533..

Thus, the usual dietary patterns are associated with the composition of the individual’s intestinal microbiota, although significant changes in the proportions of macronutrients (carbohydrates, proteins, and fats) and fibers (<25 grams/day) may induce changes in bacterial diversity and in the production of nutrients derived from bacterial metabolism55. O’Grady J, O’Connor EM, Shanahan F. Review article: dietary fibre in the era of microbiome science. Aliment Pharmacol Ther. 2019;49:506-15.. It is assumed that low fiber intake in western societies induces depletion of the gut microbiota and subsequent increases in the rates of chronic diseases such as obesity, cardiovascular disease, type 2 diabetes, colon cancer55. O’Grady J, O’Connor EM, Shanahan F. Review article: dietary fibre in the era of microbiome science. Aliment Pharmacol Ther. 2019;49:506-15., and more recently inflammatory bowel diseases66. Roda G, Chien Ng S, Kotze PG, Argollo M, Panaccione R, Spinelli A, et al. Crohn’s disease. Nat Rev Dis Primers. 2020;6:22.. Fibers are classified as soluble and insoluble and have different properties.

Soluble fiber dissolves in water, forming viscous gels, and is fermented by colonic bacteria. Highly fermentable fibers with high solubility and viscosity include beta-glucans and pectin. They are found naturally in whole grain such as oats and barley (ß-glucans) and fruits such as apples (pectin). Non-viscous soluble fibers that are fermented by the gut microbiota include inulin, gum acacia, resistant starch, polydextrose, and corn fiber77. Armet AM, Deehan EC, O’Sullivan AF, Mota JF, Field CJ, Prado CM, et al. Rethinking healthy eating in light of the gut microbiome. Cell Host Microbe. 2022;30:764-85.. Fructans of the inulin type, are found naturally in agave (a type of succulent plant), artichokes, asparagus, bananas, chicory root, garlic, onions, and leeks. Resistant starches (legumes, seeds, raw and cooked potatoes, green bananas, and whole grains) and polydextrose are not absorbed in the small intestine, as their physical and chemical characteristics make them inaccessible to α-amylase88. Wu Y, Hu H, Dai X, Che H, Zhang H. Effects of dietary intake of potatoes on body weight gain, satiety-related hormones, and gut microbiota in healthy rats. RSC Adv. 2019;9:33290-301..

Insoluble fibers do not dissolve in water, do not form gels and their fermentation is limited99. Holscher HD. Dietary fiber and prebiotics and the gastrointestinal microbiota. Gut Microbes. 2017;8:172-84.. Water-insoluble fibers have rapid gastric emptying. Cellulose is poorly fermented by intestinal bacteria, however, its presence in food accelerates intestinal transit and reduces the time of colonic bacterial fermentation of undigested foods99. Holscher HD. Dietary fiber and prebiotics and the gastrointestinal microbiota. Gut Microbes. 2017;8:172-84..

Prebiotic fibers are ingredients selectively fermented by colonic bacteria that result in specific changes in the composition and/or activity of the intestinal microbiota. This generally refers to a fiber’s ability to increase the growth of Bifidobacterium and Lactobacillus, which contribute to improving intestinal barrier function, mucus production and host immunity, reducing subpopulations of potentially pathogenic bacteria (Clostridium and Enterococcus species), acid production of short-chain fatty acids (SCFAs), acetate, propionate and butyrate, and anti-inflammatory action33. Jiang Z, Sun TY, He Y, Gou W, Zuo LS, Fu Y, et al. Dietary fruit and vegetable intake, gut microbiota, and type 2 diabetes: results from two large human cohort studies. BMC Med. 2020;18:371.,99. Holscher HD. Dietary fiber and prebiotics and the gastrointestinal microbiota. Gut Microbes. 2017;8:172-84.,1010. Armstrong H, Mander I, Zhang Z, Armstrong D, Wine E. Not All Fibers Are Born Equal; Variable Response to Dietary Fiber Subtypes in IBD. Front Pediatr. 2020;8:620189..

Resistant starch and soluble fibers such as beta glucan and pectin ferment the three SCFAs while fructans ferment butyrate, and cellulose stimulates acetate production1010. Armstrong H, Mander I, Zhang Z, Armstrong D, Wine E. Not All Fibers Are Born Equal; Variable Response to Dietary Fiber Subtypes in IBD. Front Pediatr. 2020;8:620189..

Butyrate is considered the most beneficial in terms of colonic health as it is the preferred energy source for colonic epithelial cells and promotes cell differentiation and proliferation. Butyrate-producing bacteria, mainly Eubacterium rectale, Roseburia spp, Faecalibacterium Prausnitzii, and Akkermansia muciniphila, are associated with reduced inflammation77. Armet AM, Deehan EC, O’Sullivan AF, Mota JF, Field CJ, Prado CM, et al. Rethinking healthy eating in light of the gut microbiome. Cell Host Microbe. 2022;30:764-85..

Against this context, this brief communication proposes through the food pyramid, the interactions between the intestinal microbiota, food groups, and SCFAs-producing bacteria (Figure 1).

FIGURE 1
Food pyramid and gut microbiota.

The first level of the pyramid is represented by the group of cereal, tubers, and roots. These foods are mainly a source of resistant starch, flavonoids, and polyphenols whose function for the gut microbiota is to increase the SCFAs (acetate, propionate, and butyrate), reduction of intestinal permeability, decrease the lipopolysaccharides (LPS) and endotoxemia33. Jiang Z, Sun TY, He Y, Gou W, Zuo LS, Fu Y, et al. Dietary fruit and vegetable intake, gut microbiota, and type 2 diabetes: results from two large human cohort studies. BMC Med. 2020;18:371.,77. Armet AM, Deehan EC, O’Sullivan AF, Mota JF, Field CJ, Prado CM, et al. Rethinking healthy eating in light of the gut microbiome. Cell Host Microbe. 2022;30:764-85.,88. Wu Y, Hu H, Dai X, Che H, Zhang H. Effects of dietary intake of potatoes on body weight gain, satiety-related hormones, and gut microbiota in healthy rats. RSC Adv. 2019;9:33290-301..

The second level of the pyramid is represented by the group of vegetables and fruits. The functions these foods in the gut microbiota are increasing production of SCFAs bacteria (mostly acetate and butyrate respectively), maintaining intestinal mucosal integrity, improving insulin sensitivity and anti-inflammatory properties. Furthermore, there is a decreased risk of certain cancers and reduced endotoxin-bearing Proteobacteria levels33. Jiang Z, Sun TY, He Y, Gou W, Zuo LS, Fu Y, et al. Dietary fruit and vegetable intake, gut microbiota, and type 2 diabetes: results from two large human cohort studies. BMC Med. 2020;18:371..

The third level of the pyramid includes the group of plant (beans, peas, and lentils) and animal proteins (milk and dairy products, meat, fish, and eggs). The plant beans provide resistant starch to intestinal bacteria, increasing butyrate and decreasing the levels of serum pro-inflammatory cytokines1111. Liou CS, Sirk SJ, Diaz CAC, Klein AP, Fischer CR, Higginbottom SK, et al. A Metabolic Pathway for Activation of Dietary Glucosinolates by a Human Gut Symbiont. Cell. 2020;180:717-28.e19.. The milk and dairy products produce Lactobacillus and Bifidobacterium that might suppress the growth of pathogens44. Aslam H, Marx W, Rocks T, Loughman A, Chandrasekaran V, Ruusunen A, et al. The effects of dairy and dairy derivatives on the gut microbiota: a systematic literature review. Gut Microbes. 2020;12:1799533.. The high concentrations of animal protein increase the populations of pathogens such as Escherichia coli and the lower concentrations of dietary protein decrease butyrate-producing bacteria1212. Windey K, De Preter V, Verbeke K. Relevance of protein fermentation to gut health. Mol Nutr Food Res. 2012;56:184-96.. The ideal is the daily adequacy of plant and animal proteins.

At the top of the pyramid are the groups of fats, sugars, and ultra-processed foods. These foods should be consumed in moderate amounts. High consumption of saturated fat reduces bacterial abundance, diversity, and richness, and increases body mass index (BMI) and insulin resistance1313. Wolters M, Ahrens J, Romaní-Pérez M, Watkins C, Sanz Y, Benítez-Páez A, et al. Dietary fat, the gut microbiota, and metabolic health - A systematic review conducted within the MyNewGut project. Clin Nutr. 2019;38:2504-20.. However, polyunsaturated fatty acids (PUFA), and fish and olive oil, increase the gut microbiota diversity, SCFA production, and reduce inflammation and intestinal permeability when consumed in limited amounts1414. Machate DJ, Figueiredo PS, Marcelino G, Guimarães RCA, Hiane PA, Bogo D, et al. Fatty Acid Diets: Regulation of Gut Microbiota Composition and Obesity and Its Related Metabolic Dysbiosis. Int J Mol Sci. 2020;21:4093..

Both high sugar and processed and ultra-processed foods reduce diversity bacterial, increase gut permeability, and inflammatory properties77. Armet AM, Deehan EC, O’Sullivan AF, Mota JF, Field CJ, Prado CM, et al. Rethinking healthy eating in light of the gut microbiome. Cell Host Microbe. 2022;30:764-85.. The most recent dietary guideline for the Brazilian population warns to avoid ultra-processed foods and increase natural and minimally processed foods77. Armet AM, Deehan EC, O’Sullivan AF, Mota JF, Field CJ, Prado CM, et al. Rethinking healthy eating in light of the gut microbiome. Cell Host Microbe. 2022;30:764-85.. Table 1 shows the main foods, the bacteria they produce and their role in the microbiome.

TABLE 1
The main foods, the bacteria they produce and their role in the microbiome.

The food pyramid is a pre-established nutritional education tool. The integration between the intestinal microbiome, food groups, and SCFA-producing bacteria, which benefit from the ingestion of these foods, has the potential to further improve and innovate healthy eating. The diet-microbiome interaction needs to be incorporated into nutrition science, and the food pyramid might assist in this interaction and nutritional learning.

ACKNOWLEDGEMENTS

We also would like to thank GEDIIB (Organização Brasileira de Doença de Crohn e Colite); INCT Obesidade e Diabetes CNPq (465693/2014-8) and FAPESP (2014/50907-5).

REFERENCES

  • 1
    Welsh S, Shaw A, Davis C. Achieving dietary recommendations: whole-grain foods in the Food Guide Pyramid. Crit Rev Food Sci Nutr. 1994;34:441-51.
  • 2
    Tucunduva PS, Romero LA, Rodrigues CAT, Cisotto RL. Adapted food pyramid: a guide for a right food choice. Rev. Nutr. 1999;12:65-80. doi.org/10.1590/S1415-52731999000100006
  • 3
    Jiang Z, Sun TY, He Y, Gou W, Zuo LS, Fu Y, et al. Dietary fruit and vegetable intake, gut microbiota, and type 2 diabetes: results from two large human cohort studies. BMC Med. 2020;18:371.
  • 4
    Aslam H, Marx W, Rocks T, Loughman A, Chandrasekaran V, Ruusunen A, et al. The effects of dairy and dairy derivatives on the gut microbiota: a systematic literature review. Gut Microbes. 2020;12:1799533.
  • 5
    O’Grady J, O’Connor EM, Shanahan F. Review article: dietary fibre in the era of microbiome science. Aliment Pharmacol Ther. 2019;49:506-15.
  • 6
    Roda G, Chien Ng S, Kotze PG, Argollo M, Panaccione R, Spinelli A, et al. Crohn’s disease. Nat Rev Dis Primers. 2020;6:22.
  • 7
    Armet AM, Deehan EC, O’Sullivan AF, Mota JF, Field CJ, Prado CM, et al. Rethinking healthy eating in light of the gut microbiome. Cell Host Microbe. 2022;30:764-85.
  • 8
    Wu Y, Hu H, Dai X, Che H, Zhang H. Effects of dietary intake of potatoes on body weight gain, satiety-related hormones, and gut microbiota in healthy rats. RSC Adv. 2019;9:33290-301.
  • 9
    Holscher HD. Dietary fiber and prebiotics and the gastrointestinal microbiota. Gut Microbes. 2017;8:172-84.
  • 10
    Armstrong H, Mander I, Zhang Z, Armstrong D, Wine E. Not All Fibers Are Born Equal; Variable Response to Dietary Fiber Subtypes in IBD. Front Pediatr. 2020;8:620189.
  • 11
    Liou CS, Sirk SJ, Diaz CAC, Klein AP, Fischer CR, Higginbottom SK, et al. A Metabolic Pathway for Activation of Dietary Glucosinolates by a Human Gut Symbiont. Cell. 2020;180:717-28.e19.
  • 12
    Windey K, De Preter V, Verbeke K. Relevance of protein fermentation to gut health. Mol Nutr Food Res. 2012;56:184-96.
  • 13
    Wolters M, Ahrens J, Romaní-Pérez M, Watkins C, Sanz Y, Benítez-Páez A, et al. Dietary fat, the gut microbiota, and metabolic health - A systematic review conducted within the MyNewGut project. Clin Nutr. 2019;38:2504-20.
  • 14
    Machate DJ, Figueiredo PS, Marcelino G, Guimarães RCA, Hiane PA, Bogo D, et al. Fatty Acid Diets: Regulation of Gut Microbiota Composition and Obesity and Its Related Metabolic Dysbiosis. Int J Mol Sci. 2020;21:4093.
  • 15
    Mano F, Ikeda K, Joo E, Fujita Y, Yamane S, Harada N, et al. The Effect of White Rice and White Bread as Staple Foods on Gut Microbiota and Host Metabolism. Nutrients. 2018;10:1323.
  • Disclosure of funding: no funding received

Publication Dates

  • Publication in this collection
    12 May 2023
  • Date of issue
    Jan-Mar 2023

History

  • Received
    19 July 2022
  • Accepted
    08 Dec 2022
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