Skip to main content
SpringerLink
Log in

Bioactive compounds from regular diet and faecal microbial metabolites

  • Original Contribution
  • Published:
European Journal of Nutrition Aims and scope Submit manuscript

Abstract

Purpose

Short-chain fatty acids (SCFAs) formation by intestinal bacteria is regulated by many different factors, among which dietary fibre is currently receiving most attention. However, since fibre-rich foods are usually good dietary sources of phenolic compounds, which are also known to affect the microbiota, authors hypothesize that the regular intake of these bioactive compounds could be associated with a modulation of faecal SCFA production by the intestinal microbiota.

Methods

In this work, food intake was recorded by means of a validated Food Frequency Questionnaire. Fibres were determined using Marlett food composition tables, and phenolic compounds were obtained from Phenol-Explorer Database. Analysis of SCFA was performed by gas chromatography–flame ionization/mass spectrometry and quantification of microbial populations in faeces by quantitative PCR.

Results

Klason lignin and its food contributors, as predictors of faecal butyrate production, were directly associated with Bacteroides and Bifidobacterium levels, as well as lignans with Bacteroides. Also, anthocyanidins, provided by strawberries, were associated with faecal propionate and inversely related to Lactobacillus group.

Conclusions

These results support the hypothesis we put forward regarding the association between some vegetable foods (strawberries, pasta, lentils, lettuce and olive oil) and faecal SCFA. More studies are needed in order to elucidate whether these associations have been mediated by the bacterial modulatory effect of the bioactive compounds, anthocyanins, lignans or Klason lignin, present in foodstuffs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Flint HJ, Duncan SH, Scott KP, Louis P (2015) Links between diet, gut microbiota composition and gut metabolism. Proc Nutr Soc 74(1):13–22

    Article  CAS  Google Scholar 

  2. Macfarlane S, Macfarlane GT (2003) Regulation of short-chain fatty acid production. Proc Nutr Soc 62(1):67–72

    Article  CAS  Google Scholar 

  3. Arora T, Sharma R, Frost G (2011) Propionate. Anti-obesity and satiety enhancing factor? Appetite 56(2):511–515

    Article  Google Scholar 

  4. Hosseini E, Grootaert C, Verstraete W, Van de Wiele T (2011) Propionate as a health-promoting microbial metabolite in the human gut. Nutr Rev 69(5):245–258

    Article  Google Scholar 

  5. Weitkunat K, Schumann S, Jürgen Petzke L, Blaut M, Loh G, Klaus S (2015) Effects of dietary inulin on bacterial growth, short-chain fatty acid production and hepatic lipid metabolism in gnotobiotic mice. J Nutr Biochem 26(9):929–937

    Article  CAS  Google Scholar 

  6. Wong JM, de Souza R, Kendall CW, Emam A, Jenkins DJ (2006) Colonic health: fermentation and short chain fatty acids. J Clin Gastroenterol 40(3):235–243

    Article  CAS  Google Scholar 

  7. Mallillin AC, Trinidad TP, Raterta R, Dagbay K, Loyola AS (2008) Dietary fibre and fermentability characteristics of root crops and legumes. Br J Nutr 100(3):485–488

    Article  CAS  Google Scholar 

  8. Sembries S, Dongowski G, Jacobasch G, Mehrlander K, Will F, Dietrich H (2003) Effects of dietary fibre-rich juice colloids from apple pomace extraction juices on intestinal fermentation products and microbiota in rats. Br J Nutr 90(3):607–615

    Article  CAS  Google Scholar 

  9. Cuervo A, Salazar N, Rúas-Madiedo P, Gueimonde M, González S (2013) Fiber from a regular diet is directly associated with fecal short-chain fatty acid concentrations in the elderly. Nutr Res 33(10):811–816

    Article  CAS  Google Scholar 

  10. Topping DL, Clifton PM (2001) Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiol Rev 81(3):1031–1064

    Article  CAS  Google Scholar 

  11. Cuervo A, Valdés L, Salazar N, de los Reyes-Gavilán CG, Rúas-Madiedo P, Gueimonde M et al (2014) Pilot study of diet and microbiota: interactive associations of fibers and polyphenols with human intestinal bacteria. J Agric Food Chem 62(23):5330–5336

    Article  CAS  Google Scholar 

  12. Queipo-Ortuño MI, Boto-Ordoñez M, Murri M, Gómez-Zumaquero JM, Clemente-Postigo M, Estruch R et al (2012) Influence of red wine polyphenols and ethanol on the gut microbiota ecology and biochemical biomarkers. Am J Clin Nutr 95(6):1323–1334

    Article  Google Scholar 

  13. Cuervo A, Hevia A, López P, Suárez A, Sánchez B, Margolles A et al (2015) Association of polyphenols from oranges and apples with specific intestinal microorganisms in systemic lupus erythematosus patients. Nutrients 7(2):1301–1317

    Article  CAS  Google Scholar 

  14. Shinohara K, Ohashi Y, Kawasumi K, Terada A, Fujisawa T (2010) Effect of apple intake on fecal microbiota and metabolites in humans. Anaerobe 16(5):510–515

    Article  CAS  Google Scholar 

  15. Massot-Cladera M, Abril-Gil M, Torres S, Franch A, Castell M, Perez-Cano FJ (2014) Impact of cocoa polyphenol extracts on the immune system and microbiota in two strains of young rats. Br J Nutr 112:1944–1954. doi:10.1017/S0007114514003080

    Article  CAS  Google Scholar 

  16. Massot-Cladera M, Costabile A, Childs CE, Yaqoob P, Franch A, Castell M, Perez-Cano FJ (2015) Prebiotic effects of cocoa fibre on rats. J Funct Foods 19:341–352

    Article  CAS  Google Scholar 

  17. Jang S, Sun J, Chen P, Lakshman S, Molokin A, Harnly JM, Vinyard BT, Urban JF Jr, Davis CD, Solano-Aguilar G (2016) Flavanol-enriched cocoa powder alters the intestinal microbiota, tissue and fluid metabolite profiles, and intestinal gene expression in pigs. J Nutr 146:673–680

    Article  CAS  Google Scholar 

  18. Unno T, Hisada T, Takahashi S (2015) Hesperetin modifies the composition of fecal microbiota and increases cecal levels of short-chain fatty acids in rats. J Agric Food Chem 63(36):7952–7957

    Article  CAS  Google Scholar 

  19. Wu GD, Chen J, Hoffmann C, Bittinger K, Chen Y, Keilbaugh SA, Bewtra M, Knights D, Walters WA, Knight R, Sinha R, Gilroy E, Gupta K, Baldassano R, Nessel L, Li H, Bushman FD, Lewis JD (2011) Linking long-term dietary patterns with gut microbial enterotypes. Science 334(6052):105–108. doi:10.1126/science.1208344

    Article  CAS  Google Scholar 

  20. Centro de Enseñanza Superior de Nutrición Humana y Dietética (2008) Tablas de Composición de Alimentos por Medidas Caseras de Consumo Habitual en España. McGraw Hill, Publicaciones y ediciones de la Universidad de Barcelona, Barcelona

  21. United State Department of Agriculture (USDA). Agricultural Research Service (2016) USDA National Nutrient Database for Standard Reference. http://www.ars.usda.gov/services/docs.htm?docid=8964. Accessed 5 Oct 2016

  22. Marlett JA, Cheung TF (1997) Database and quick methods of assessing typical dietary fiber intakes using data for 228 commonly consumed foods. J Am Diet Assoc 97(10):1139–1151

    Article  CAS  Google Scholar 

  23. Theander O, Westerlund EA (1986) Studies on dietary fiber, 3: improved procedures for analysis of dietary fiber. J Agric Food Chem 34:330–336

    Article  CAS  Google Scholar 

  24. Seaman JF (1945) Kinetics of wood saccharification: hydrolysis of cellulose and decomposition of sugars in dilute acid at high temperature. Ind Eng Chem 37:43–52

    Article  Google Scholar 

  25. Neveu V, Perez-Jimenez J, Vos F, Crespy V, du CL, Mennen L et al (2010) Phenol-Explorer: an online comprehensive database on polyphenol contents in foods. Database 2010. http://phenol-explorer.eu/. doi:10.1093/database/bap024. Accessed 5 Oct 2016

  26. Salazar N, López P, Valdés L, Margolles A, Suárez A, Patterson AM et al (2013) Microbial targets for the development of functional foods accordingly with nutritional and immune parameters altered in the elderly. J Am Coll Nutr 32(6):399–406

    Article  CAS  Google Scholar 

  27. Arboleya S, Binetti A, Salazar N, Fernández N, Solís G, Hernández-Barranco A et al (2012) Establishment and development of intestinal microbiota in preterm neonates. FEMS Microbiol Ecol 79(3):763–772

    Article  CAS  Google Scholar 

  28. Cuervo A, de los Reyes-Gavilán CG, Rúas-Madiedo P, López P, Suárez A, Gueimonde M, González S (2015) Red wine consumption is associated with fecal microbiota and malondialdehyde in a human population. J Am Col Nutr 34:135–141

    Article  CAS  Google Scholar 

  29. Vijay-Kumar M, Aitken JD, Carvalho FA, Cullender TC, Mwangi S, Srinivasan S et al (2010) Metabolic syndrome and altered gut microbiota in mice lacking toll-like receptor 5. Science 328(5975):228–231

    Article  CAS  Google Scholar 

  30. Maslowski KM, Vieira AT, Ng A, Kranich J, Sierro F, Yu D et al (2009) Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 461(7268):1282–1286

    Article  CAS  Google Scholar 

  31. Scott KP, Duncan SH, Louis P, Flint HJ (2011) Nutritional influences on the gut microbiota and the consequences for gastrointestinal health. Biochem Soc Trans 39(4):1073–1078

    Article  CAS  Google Scholar 

  32. Ríos-Covián D, Gueimonde M, Duncan SH, Flint HJ, de los Reyes-Gavilán CG (2015) Enhanced butyrate formation by cross-feeding between Faecalibacterium prausnitzii and Bifidobacterium adolescentis. FEMS Microbiol Lett. doi:10.1093/femsle/fnv176

    Google Scholar 

  33. Scott KP, Gratz SW, Sheridan PO, Flint HJ, Duncan SH (2013) The influence of diet on the gut microbiota. Pharmacol Res 69(1):52–60

    Article  CAS  Google Scholar 

  34. Flint HJ, Bayer EA, Rincon MT, Lamed R, White BA (2008) Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nat Rev Microbiol 6(2):121–131

    Article  CAS  Google Scholar 

  35. Duncan SH, Louis P, Flint HJ (2004) Lactate-utilizing bacteria, isolated from human feces, that produce butyrate as a major fermentation product. Appl Environ Microbiol 70(10):5810–5817

    Article  CAS  Google Scholar 

  36. Tanaka S, Yamamoto K, Yamada K, Furuya K, Uyeno Y (2016) Relationship of enhanced butyrate production by colonic butyrate-producing bacteria to immunomodulatory effects in normal mice fed an insoluble fraction of Brassica rapa L. Appl Environ Microbiol 82(9):2693–2699

    Article  CAS  Google Scholar 

  37. Morrison DJ, Mackay WG, Edwards CA, Preston T, Dodson B, Weaver LT (2006) Butyrate production from oligofructose fermentation by the human faecal flora: what is the contribution of extracellular acetate and lactate? Br J Nutr 96(3):570–577

    CAS  Google Scholar 

  38. Clavel T, Borrmann D, Braune A, Dore J, Blaut M (2006) Occurrence and activity of human intestinal bacteria involved in the conversion of dietary lignans. Anaerobe 12(3):140–147

    Article  CAS  Google Scholar 

  39. Prasad K (2001) Secoisolariciresinol diglucoside from flaxseed delays the development of type 2 diabetes in Zucker rat. J Lab Clin Med 138(1):32–39

    Article  CAS  Google Scholar 

  40. Zamora-Ros R, Knaze V, Rothwell JA, Hemon B, Moskal A, Overvad K et al (2016) Dietary polyphenol intake in Europe: The European Prospective Investigation into Cancer and Nutrition (EPIC) study. Eur J Nutr 55(4):1359–1375

    Article  CAS  Google Scholar 

  41. Tresserra-Rimbau A, Medina-Remon A, Perez-Jimenez J, Martinez-Gonzalez MA, Covas MI, Corella D et al (2013) Dietary intake and major food sources of polyphenols in a Spanish population at high cardiovascular risk: the PREDIMED study. Nutr Metab Cardiovasc Dis 23(10):953–959

    Article  CAS  Google Scholar 

  42. Ovaskainen ML, Torronen R, Koponen JM, Sinkko H, Hellstrom J, Reinivuo H et al (2008) Dietary intake and major food sources of polyphenols in finnish adults. J Nutr 138(3):562–566

    Article  CAS  Google Scholar 

  43. Valdés L, Cuervo A, Salazar N, Ruas-Madiedo P, Gueimonde M, González S (2015) The relationship between phenolic compounds form diet and microbiota: impact on human health. Food Funct 6:2424–2439

    Article  Google Scholar 

  44. Dueñas M, Cueva C, Muñóz-González I, Jiménez-Girón A, Sánchez-Patán F, Santos-Buelga C, Moreno-Arribas MV, Bartolomé B (2015) Studies on modulation of gut microbiota by wine polyphenols: from isolated cultures to omic approaches. Antioxidants 4:1–21

    Article  Google Scholar 

  45. Perez-Jimenez J, Fezeu L, Touvier M, Arnault N, Manach C, Hercberg S et al (2011) Dietary intake of 337 polyphenols in French adults. Am J Clin Nutr 93(6):1220–1228

    Article  CAS  Google Scholar 

  46. Lin HV, Frassetto A, Kowalik EJ Jr, Nawrocki AR, Lu MM, Kosinski JR et al (2012) Butyrate and propionate protect against diet-induced obesity and regulate gut hormones via free fatty acid receptor 3-independent mechanisms. PLoS One 7(4):e35240. doi:10.1371/journal.pone.0035240

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This study was financed by the Spanish Plan Nacional de I+D (Grant AGL2010-14952) and by Biópolis SL. within the framework of the e-CENIT Project SENIFOOD from the Spanish Ministry of Science and Innovation. The activity of the group is being partly supported through the Grant GRUPIN14-043 from “Plan Regional de Investigación” of Principado de Asturias. Both AGL2010-14952 and GRUPIN14-043 received cofounding from European Union FEDER funds. N. Salazar benefits from a “Clarín” postdoctoral contract (Marie Curie European CoFund Program) co-funded by the “Plan Regional de Investigación” of Principado de Asturias, Spain. B. Sánchez was the recipient of a “Ramón y Cajal” postdoctoral contract from the Spanish Ministry of Economy and Competitiveness. The contract of I. Gutierrez-Diaz was supported by grant GRUPIN14-043. We acknowledge the excellent technical assistance of Lidia Alaez, whose contract was partially supported by the Project AGL2010-16525 and by “Plan Regional de Investigación” of Principado de Asturias, through the Grant COF 13-020. We show our greatest gratitude to all the volunteers participating in the study and to “Alimerka Foundation”.

Author information

Authors and Affiliations

  1. Department of Functional Biology, University of Oviedo, C/Julián Clavería s/n, 33006, Oviedo, Asturias, Spain

    Tania Fernández-Navarro, Isabel Gutiérrez-Díaz & Sonia González

  2. Department of Microbiology and Biochemistry of Dairy Products, Instituto de Productos Lácteos de Asturias - Consejo Superior de Investigaciones Científicas (IPLA-CSIC), Paseo Río Linares s/n, 33300, Villaviciosa, Asturias, Spain

    Tania Fernández-Navarro, Nuria Salazar, Isabel Gutiérrez-Díaz, Borja Sánchez, Patricia Rúas-Madiedo, Clara G. de los Reyes-Gavilán, Abelardo Margolles & Miguel Gueimonde

Authors
  1. Tania Fernández-Navarro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nuria Salazar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Isabel Gutiérrez-Díaz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Borja Sánchez
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Patricia Rúas-Madiedo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Clara G. de los Reyes-Gavilán
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Abelardo Margolles
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Miguel Gueimonde
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Sonia González
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sonia González.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest. The founding sponsors had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; and in the decision to publish the results.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fernández-Navarro, T., Salazar, N., Gutiérrez-Díaz, I. et al. Bioactive compounds from regular diet and faecal microbial metabolites. Eur J Nutr 57, 487–497 (2018). https://doi.org/10.1007/s00394-016-1332-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00394-016-1332-8

Keywords

Search

Navigation