Skip to main content
SpringerLink
Log in

Factors affecting the conversion of apple polyphenols to phenolic acids and fruit matrix to short-chain fatty acids by human faecal microbiota in vitro

  • ORIGINAL CONTRIBUTION
  • Published:
European Journal of Nutrition Aims and scope Submit manuscript

Abstract

Proanthocyanidins (PAs) in apples are condensed tannins comprised mostly of (−)-epicatechin units with some terminal (+)-catechins. PAs, especially those having a long chain-length, are absorbed in the upper intestine only to a small extent and are passed to the colon. In the colon they are subjected to microbial metabolism by colonic microbiota. In the present article, the ability of human microbiota to ferment apple PAs is studied. Freeze-dried fruit preparations (apple, enzymatically digested apple, isolated cell-walls, isolated PAs or ciders) from two varieties, Marie Ménard and Avrolles, containing PAs of different chain lengths, were compared. Fermentation studies were performed in an in vitro colon model using human faecal microbiota as an inoculum. The maximal extent of conversion to known microbial metabolites, was observed at late time point for Marie Ménard cider, having short PAs. In this case, the initial dose also contributed to the extent of conversion. Long-chain PAs were able to inhibit the in vitro microbial metabolism of PAs shown as low maxima at early time points. Presence of isolated PAs also suppressed SCFA formation from carbohydrates as compared with that from apple cell wall or faecal suspension without substrates. The low maximal extents at early time points suggest that there is a competition between the inhibitory effect of the PAs on microbial activity, and the ability to convert PAs by the microbiota.

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
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Abia R, Fry SC (2001) Degradation and metabolism of 14C-labeled proanthocyanidins from carob (Ceratonia siliqua) pods in the gastrointestinal tract of the rat. J Sci Food Agric 81:1156–1165

    Article  CAS  Google Scholar 

  2. Aprikian O, Duclos V, Guyot S, Besson C (2003) Apple pectin and a polyphenol-rich apple concentrate are more effective together than separately on cecal fermentations and plasma lipids in rats. J Nutr 133:1860–1865

    CAS  Google Scholar 

  3. Auger C, Al-Awwadi N, Bornet A, Rouanet J-M, Gasc F, Cros G, Teissedre P-L (2004) Catechins and procyanidins in Mediterranean diets. Food Res Intern 37:233–245

    Article  CAS  Google Scholar 

  4. Aura A-M, Härkönen H, Fabritius M, Poutanen K (1999) Development of an in vitro digestion method for removal of starch and protein and assessment of its performance using rye and wheat breads. J Cereal Sci 29:139–152

    Article  CAS  Google Scholar 

  5. Aura A-M, O’Leary KA, Williamson G, Ojala M, Bailey M, Puupponen-Pimiä R, Nuutila AM, Oksman-Caldentey K-M, Poutanen K (2002) Quercetin derivatives are conjugated and converted to hydroxyphenylacetic acid but not methylated by human fecal flora in vitro. J Agric Food Chem 50:1725–1730

    Article  CAS  Google Scholar 

  6. Aura A-M, Karppinen S, Virtanen H, Forssell P, Heinonen S-M, Nurmi T, Adlercreutz H, Poutanen K (2005) Processing of rye bran influences both the fermentation of dietary fibre and the bioconversion of lignans by human faecal flora in vitro. J Sci Food Agric 85:2085–2093

    Article  CAS  Google Scholar 

  7. Aura A-M, Mattila I, Seppänen-Laakso T, Miettinen J, Oksman-Caldentey K-M, Oresic M (2008) Microbial metabolism of catechin stereoisomers by human faecal microbiota: comparison of targeted analysis and a non-targeted metabolomics method. Phytochem Lett 1:18–22

    Article  Google Scholar 

  8. Barry JL, Hoebler C, Macfarlane GT, Macfarlane S, Mathers JC, Reed KA, Mortensen PB, Norgaard I, Rowland IR, Rumney CJ (1995) Estimation of the fermentability of dietary fibre in vitro: a European interlaboratory study. Br J Nutr 74:303–322

    Article  CAS  Google Scholar 

  9. Blumenkrantz N, Asboe-Hansen G (1973) New method for quantitative determination of uronic acids. Anal Biochem 54:484–489

    Article  CAS  Google Scholar 

  10. Cerda B, Tomas-Barberan FA, Espin JC (2005) Metabolism of antioxidant and chemopreventive ellagitannins from strawberries, raspberries, walnuts, and oak-aged wine in humans: identification of biomarkers and individual variability. J Agric Food Chem 53:227–235

    Article  CAS  Google Scholar 

  11. Cheynier V, Prieur C, Guyot S, Rigaud J, Moutounet M (1997) The structures of tannins in grapes and wines and their interactions with proteins. In: Watkins T (ed) Wine; nutritional and therapeutic benefits. ACS Symp Series 661:81–93

  12. Deprez S, Brezillon C, Rabot S, Philippe C, Mila I, Lapierre C, Scalbert A (2000) Polymeric proanthocyanidins are catabolized by human colonic microflora into low-molecular-weight phenolic acids. J Nutr 130:2733–2738

    CAS  Google Scholar 

  13. Englyst HN, Cummings JH (1984) Simplified method for the measurement of total non-starch polysaccharides by gas-liquid chromatography of constituent sugars as alditol acetates. Analyst 109:937–942

    Article  CAS  Google Scholar 

  14. Gonthier M-P, Donovan JL, Texier O, Felgines C, Remesy C, Scalbert A (2003) Metabolism of dietary procyanidins in rats. Free Radical Bio Biochem 35:837–844

    Article  CAS  Google Scholar 

  15. Gonthier M-P, Remesy C, Scalbert A, Cheynier V, Souquet J-M, Poutanen K, Aura A-M (2006) Microbial metabolism of caffeic acid and its esters chlorogenic and caftaric acids by human faecal microbiota in vitro. Biomed Pharmacother 60:536–540

    Article  CAS  Google Scholar 

  16. Guyot S, Marnet N, Sanoner P, Drilleau J-F (2001) Direct thiolysis on crude apple materials for high-performance liquid chromatography characterization and quantification of polyphenols in cider apple tissues and juices. In: Packer L (ed) Methods in enzymology—flavonoïds and other polyphenols. Academic Press, New York 335:57–70

  17. Guyot S, Marnet N, Drilleau JF (2001) Thiolysis-HPLC characterization of apple procyanidins covering a large range of polymerization states. J Agric Food Chem 49:2085–2093

    Article  Google Scholar 

  18. Guyot S, Le Bourvellec C, Marnet N, Drilleau JF (2002) Procyanidins are the most abundant polyphenols in dessert apples at maturity. Lebensm U-Wiss Technol 35:289–291

    Article  CAS  Google Scholar 

  19. Guyton AC, Hall JE (1996) Transport and mixing of food in the alimentary tract. In: Textbook of medical physiology, 9th edn. W.B. Saunders Company, Philadelphia pp 803–813

  20. Hammerstone JF, Lazarus SA, Schmitz HH (2000) Procyanidin content and variation in some commonly consumed foods. J Nutr 130:2086S–2092S

    CAS  Google Scholar 

  21. Holt RR, Lazarus SA, Sullards MC, Zhu QY, Schramm DD, Hammerstone JF, Fraga CG, Schmitz HH, Keen CL (2002) Procyanidin dimer B2 [epicatechin-(4B-8)-epicatechin] in human plasma after consumption of a flavanol-rich cocoa. Am J Clin Nutr 76:798–804

    CAS  Google Scholar 

  22. Hubert B, Baron A, Le Queré J-M, Renard CMGC (2007) Influence of prefermentary clarification on the composition of apple musts. J Agric Food Chem 55:5118–5122

    Article  CAS  Google Scholar 

  23. Johnson IT (2002) Anticarcinogenic effects of diet-related apoptosis in the colorectal mucosa. Food Chem Toxicol 40:1171–1178

    Article  CAS  Google Scholar 

  24. Lafay S, Gil-Izquierdo A (2008) Bioavailability of phenolic acids. Phytochem Rev 7:301–311

    Article  CAS  Google Scholar 

  25. Le Bourvellec C, Le Quéré J-M, Renard CMGC (2007) Impact of non-covalent interactions between condensed tannin and apple cell-walls: elaboration of a quantitative model and its application to transfer from fruit to juice. J Agric Food Chem 55:7896–7904

    Article  CAS  Google Scholar 

  26. Lea AGH (1978) The analysis of cider phenolics. Ann Nutr Alim 32:1051–1061

    CAS  Google Scholar 

  27. Levrat M-A, Texier MDO, Régerat F, Demingé C, Rémésy C (1993) Comparison of the effects of condensed tannin and pectin cecal fermentations and lipid metabolism in the rat. Nutr Res 13:427–433

    Article  CAS  Google Scholar 

  28. Mangas JJ, Moreno J, Rodriguez R, Picinelli A, Suarez B (1999) Analysis of polysaccharides in cider: their effect on sensory foaming properties. J Agric Food Chem 47:152–156

    Article  CAS  Google Scholar 

  29. McDougall GJ, Stewart D (2005) The inhibitory effects of berry polyphenols on digestive enzymes. BioFactors 23:185–195

    Google Scholar 

  30. Meselhy MR, Nakamura N, Hattori M (1997) Biotransformation of (−)-epicatechin-3-gallate by human intestinal bacteria. Chem Pharm Bull 45:888–893

    CAS  Google Scholar 

  31. Minekus M, Smeets-Peters M, Bernalier A, Marol-Bonnin S, Havenaar R, Marteau P, Altric M, Fonty G, Huis in′t Veld JHJ (1999) A computer-controlled system to simulate conditions of the large intestine with peristaltic mixing, water absorption and adsorption of fermentation products. Appl Microbiol Biotechnol 53:108–114

    Article  CAS  Google Scholar 

  32. Olano-Martin E, Mountzouris KC, Gibson GR, Rastall RA (2000) In vitro fermentability of dextran, oligodextran and maltodextrin by human gut bacteria. Br J Nutr 83:247–255

    CAS  Google Scholar 

  33. Pinent M, Bladé C, Salvadó MJ, Blay M, Pujadas G, Fernández-Larrea J, Arola L, Ardévol A (2006) Procyanidin effects on adipocyte-related pathologies. Crit Rev Food Sci Nutr 46:543–550

    Article  CAS  Google Scholar 

  34. Plumb GW, Garcia-Gonesa MT, Kroon PA, Rhodes M, Ridley S, Williamson G (1999) Metabolism of chlorogenic acid by human plasma, liver, intestine and gut microbiota. J Sci Food Agric 79:390–392

    Article  CAS  Google Scholar 

  35. Puupponen-Pimiä R, Nohynek L, Alakomi H-L, Oksman-Caldentey K-M (2005) Bioactive berry compounds–novel tools against human pathogens. Appl Micobiol Biotechnol 67:8–18

    Article  Google Scholar 

  36. Renard CMGC (2005) Variability in cell-wall preparations: quantification and comparison of common methods. Carbohydr Polym 60:515–522

    Article  CAS  Google Scholar 

  37. Renard CMGC, Baron A, Guyot S, Drilleau J-F (2001) Interactions between apple cell-walls and native apple polyphenols: quantification and some consequences. Int J Biol Macromol 29:115–125

    Article  CAS  Google Scholar 

  38. Renard CMGC, Dupont N, Guillermin P (2007) Concentrations and characteristics of procyanidins and other phenolics in apples during fruit growth. Phytochemistry 68:1128–1138

    Article  CAS  Google Scholar 

  39. Rios LY, Gonthier M-P, Rémésy C, Mila I, Lapierre C, Lazarus SA, Williamson G, Scalbert A (2003) Chocolate intake increases urinary excretion of polyphenol-derived phenolic acids in healthy human subjects. Am J Clin Nutr 77:912–918

    CAS  Google Scholar 

  40. Sano A, Yamakoshi J, Tokukake S, Tobe K, Kubota Y, Kikuchi M (2003) Procyanidin B1 is detected in human serum after intake of proanthocyanidin-rich grape seed extract. Biosci Biotechnol Biochem 67:1140–1143

    Article  CAS  Google Scholar 

  41. Sanoner P, Guyot S, Marnet N, Molle D, Drilleau JF (1999) Polyphenolic profiles of French cider apple varieties. J Agric Food Chem 47:4847–4853

    Article  CAS  Google Scholar 

  42. Scalbert A (1991) Antimicrobial properties of tannins. Phytochemistry 30:3875–3883

    Article  CAS  Google Scholar 

  43. Seaman JF, Moore WE, Mitchell RL, Millett MA (1954) Techniques for the determination of pulp constituents by quantitative paper chromatography. TAPPI 37:336–343

    Google Scholar 

  44. Shoji T, Masumoto S, Moriichi N, Akiyama H, Kanda T, Ohtake Y, Goda Y (2006) Apple procyanidin oligomers absorption in rats after oral administration: analysis of procyanidins in plasma using the Potter method and high-performance liquid chromatography/tandem mass spectrometry. J Agric Food Chem 54:884–892

    Article  CAS  Google Scholar 

  45. Siebert KJ, Carrasco A, Lynn PY (1996) Formation of protein-polyphenol haze in beverages. J Agric Food Chem 44:1997–2005

    Article  CAS  Google Scholar 

  46. Sivakumaran S, Molan AL, Meagher LP, Kolb B, Foo LY, Lane GA, Attwood GA, Fraser K, Tavendale M (2004) Variation in antimicrobial action of proanthocyanidins from Dorycnium rectum against rumen bacteria. Phytochemistry 65:2485–2497

    Article  CAS  Google Scholar 

  47. Tomaru M, Takano H, Osakabe N, Yasuda A, Inoue K, Yanagisawa R, Ohwatari T, Uematsu H (2007) Dietary supplementation with cacao liquor proanthocyanidins prevents elevation of blood glucose levels in diabetic obese mice. Nutrition 23:351–355

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Hannele Virtanen is thanked for conducting SCFA analysis. Annika Majanen, Siv Matomaa, Marita Ikonen and Airi Hyrkäs are gratefully acknowledged for the skilful technical assistance. Dr Riitta Puupponen-Pimiä is thanked for fruitful comments on the manuscript. European Commission (STREP-FLAVO Food-CT-2004-513960) is acknowledged for financial support for the study.

Author information

Authors and Affiliations

  1. VTT, Technical Research Center of Finland, P.O. Box 1000, Tietotie 2, 02044 VTT, Finland

    Sarah Bazzocco, Ismo Mattila & Anna-Marja Aura

  2. INRA, UR117, Rennes, France

    Sylvain Guyot

  3. INRA, UMR408, Avignon, France

    Catherine M. G. C. Renard

Authors
  1. Sarah Bazzocco
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ismo Mattila
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sylvain Guyot
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Catherine M. G. C. Renard
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Anna-Marja Aura
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anna-Marja Aura.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bazzocco, S., Mattila, I., Guyot, S. et al. Factors affecting the conversion of apple polyphenols to phenolic acids and fruit matrix to short-chain fatty acids by human faecal microbiota in vitro . Eur J Nutr 47, 442–452 (2008). https://doi.org/10.1007/s00394-008-0747-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00394-008-0747-2

Keywords

Search

Navigation