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Applied Microbiology and Biotechnology

, Volume 67, Issue 1, pp 8–18 | Cite as

Bioactive berry compounds—novel tools against human pathogens

  • Riitta Puupponen-PimiäEmail author
  • Liisa Nohynek
  • Hanna-Leena Alakomi
  • Kirsi-Marja Oksman-Caldentey
Mini-Review

Abstract

Berry fruits are rich sources of bioactive compounds, such as phenolics and organic acids, which have antimicrobial activities against human pathogens. Among different berries and berry phenolics, cranberry, cloudberry, raspberry, strawberry and bilberry especially possess clear antimicrobial effects against, e.g. Salmonella and Staphylococcus. Complex phenolic polymers, like ellagitannins, are strong antibacterial agents present in cloudberry and raspberry. Several mechanisms of action in the growth inhibition of bacteria are involved, such as destabilisation of cytoplasmic membrane, permeabilisation of plasma membrane, inhibition of extracellular microbial enzymes, direct actions on microbial metabolism and deprivation of the substrates required for microbial growth. Antimicrobial activity of berries may also be related to antiadherence of bacteria to epithelial cells, which is a prerequisite for colonisation and infection of many pathogens. Antimicrobial berry compounds may have important applications in the future as natural antimicrobial agents for food industry as well as for medicine. Some of the novel approaches are discussed.

Keywords

Tannin Lactic Acid Bacterium EGCG Ellagic Acid Carvacrol 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

The authors thank Professor Veli Kauppinen for his ideas and valuable discussions during the berry research at VTT. The secretarial work of Oili Lappalainen is gratefully acknowledged. Tekes, the National Technology Agency is acknowledged for financial support through the berry projects during the years 1998–2000 and 2001–2004.

References

  1. Akiyama H, Fujii K, Yamasaki O, Oono T, Iwatsuki K (2001) Antibacterial action of several tannins against Staphylococcus aureus. J Antimicrob Chemother 48:487–491CrossRefPubMedGoogle Scholar
  2. Alakomi H-L, Skyttä E, Saarela M, Mattila-Sandholm T, Latva-Kala K, Helander IM (2000) Lactic acid permeabilizes gram-negative bacteria by disrupting the outer membrane. Appl Environ Microbiol 66:2001–2005CrossRefPubMedGoogle Scholar
  3. Alakomi H-L, Saarela M, Helander I (2003) Effect of EDTA on Salmonella enterica serovar Typhimurium involves a component not assignable to lipopolysaccharide release. Microbiology 149:2015–2021CrossRefPubMedGoogle Scholar
  4. Alberto MR, Farias ME, Manca de Nadra MC (2001) Effect of gallic acid and cathechin on Lactobacillus hilgardii 5w growth and metabolism of organic compounds. J Agric Food Chem 49:4359–4363CrossRefPubMedGoogle Scholar
  5. Aruoma OI, Murcia A, Butler J, Halliwell B (1993) Evaluation of the antioxidant and prooxidant actions of gallic acid and its derivatives. J Agric Food Chem 41:1880–1885Google Scholar
  6. Audia JP, Webb CC, Foster JW (2001) Breaking through the acid barrier: an orchestrated response to proton stress by enteric bacteria. Int J Med Microbiol 291:97–106PubMedGoogle Scholar
  7. Barber MS, McConnell VS, DeCaux B (2000) Antimicrobial intermediates of the general phenylpropanoid and lignin specific pathways. Phytochemistry 54:53–56CrossRefPubMedGoogle Scholar
  8. Bate-Smith EC (1973) Haemanalysis of tannins: the concept of relative astringency. Phytochemistry 12:907–912CrossRefGoogle Scholar
  9. Belofsky G, Percivill D, Lewis K, Tegos GP, Ekart J (2004) Phenolic metabolites of Dalea versicolor that enhance antibiotic activity against model pathogenic bacteria. J Nat Prod 67:481–484CrossRefPubMedGoogle Scholar
  10. Beuchat LR, Heaton EK (1975) Salmonella survival on pecan as influenced by processing and storage conditions. Appl Microbiol 29:795–801PubMedGoogle Scholar
  11. Brul S, Coote P (1999) Preservative agents in foods. Mode of action and microbial resistance mechanisms. Int J Food Microbiol 50:1–17Google Scholar
  12. Burger O, Weiss E, Sharon N, Tabak M, Neeman I, Ofek I (2002) Inhibition of Helicobacter pylori adhesion to human gastric mucus by a high-molecular-weight constituent of cranberry juice. Crit Rev Food Sci Nutr 42 [Suppl]:279–284PubMedGoogle Scholar
  13. Burt S (2004) Essential oils: their antibacterial properties and potential applications in foods—a review. Int J Food Microbiol 94:223–253CrossRefPubMedGoogle Scholar
  14. Campos FM, Couto JA, Hogg TA (2003) Influence of phenolic acids on growth and inactivation of Oenococcus oeni and Lactobacillus hilgardii. J Appl Microbiol 94:167–174CrossRefPubMedGoogle Scholar
  15. Caturla N, Vera-Samper E, Villalain J, Mateo CR, Micol V (2003) The relationship between the antioxidant and antibacterial properties of galloylated catechins and the structure of phospholipid model membranes. Free Radical Biol Med 34:648–662CrossRefGoogle Scholar
  16. Cavanagh HM, Hipwell M, Wilkinson JM (2003) Antibacterial activity of berry fruits used for culinary purposes. J Med Food 1:57–61CrossRefGoogle Scholar
  17. Chung K-T, Stevens SE, Jr, Lin W-F, Wei CI (1993) Growth inhibition of selected food-borne bacteria by tannic acid, propyl gallate and related compounds. Lett Appl Microbiol 17:29–32Google Scholar
  18. Chung K-T, Lu Z, Chou MW (1998a) Mechanism of inhibition of tannic acid and related compounds on the growth of intestinal bacteria. Food Chem Toxicol 36:1053–1060CrossRefPubMedGoogle Scholar
  19. Chung K-T, Wei C-I, Johnson MG (1998b) Are tannins a double-edged sword in biology and health? Trends Food Sci Technol 9:168–175CrossRefGoogle Scholar
  20. Cotter PD, Hill C (2003) Surviving the acid test: responses of Gram-positive bacteria to low pH. Microbiol Mol Biol Rev 67:429–453CrossRefPubMedGoogle Scholar
  21. Doores S (1993) Organic acids. In: Davidson PM, Branen AL (eds) Antimicrobials in food, 2nd edn. Marcel Dekker, New York, pp 95–136Google Scholar
  22. Friedman M, Jürgens HS (2000) Effect of pH on the stability of plant phenolic compounds. J Agric Food Chem 48:2101–2110CrossRefPubMedGoogle Scholar
  23. Hada N, Kakiuchi N, Hattori M, Namba T (1989) Identification of antibacterial principles against Streptococcus mutans inhibitory principles against glucosyltransferase from the seed of Areca catechu L. Phytother Res 3:140–144Google Scholar
  24. Haddock EA, Gupta RK, Al-Shafi SMK, Layden K, Haslam E, Magnolato D (1982) The metabolism of gallic acid and hexahydroxydiphenic acids in plants: Biogenetic and molecular taxonomic considerations. Phytochemistry 5:1049–1062CrossRefGoogle Scholar
  25. Harmand MF, Blanquet P (1978) The fate of total flavonolic oligomers (OFT) extracted from Vitis vinifera L. in the rat. Eur J Drug Metab Pharmacokinet 1:15–30Google Scholar
  26. Haslam E (1989) Plant polyphenols: vegetable tannins revisited. Cambridge University Press, CambridgeGoogle Scholar
  27. Hatano T, Kusuda M, Hori M, Shiota S, Tsuchiya T, Yoshida T (2003) Theasinensin A, a tea polyphenol formed from (-)-epigallocatechin gallate, suppresses antibiotic resistance of methicillin-resistant Staphylococcus aureus. Planta Med 69:984–989CrossRefPubMedGoogle Scholar
  28. Helander I, Alakomi H-L, Latva-Kala K, Mattila-Sandholm T, Pol I, Smid E, Gorris L, Wright von A (1998) Characterization of the action of selected essential oil components on gram-negative bacteria. J Agric Food Chem 46:3590–3595CrossRefGoogle Scholar
  29. Helander IM, Mattila-Sandholm T (2000) Fluorometric assessment of Gram-negative bacterial permeabilization. J Appl Microbiol 88:213–219CrossRefPubMedGoogle Scholar
  30. Herald PJ, Davidson PM (1983) Antibacterial activity of selected hydroxycinnamic acids. J Food Sci 48:1378–1379Google Scholar
  31. Herrmann K (1989) Occurence and content of hydroxycinnamic and hydroxybenzoic acid compounds in foods. Crit Rev Food Sci Nutr 28:315–347PubMedGoogle Scholar
  32. Howell AB (2002) Cranberry proanthocyanidins and the maintenance of urinary tract health. Crit Rev Food Sci Nutr 42 [Suppl]:273–278PubMedGoogle Scholar
  33. Howell AB, Vorsa N, Marderosian AD, Foo LY (1998) Inhibition of the adherence of P-fimbriated Escherichia coli to uro-epithelial surfaces by proanthycyanidin extracts from cranberries. NE J Med 339:1085–1086CrossRefGoogle Scholar
  34. Howell AB, Leahy M, Kurowska E, Guthrie N (2001) In vivo evidence that cranberry proanthocyanidins inhibit adherence of P-fimbriated E. coli bacteria to uroepithelial cells. FASEB J 15(4):A284Google Scholar
  35. Hu Z-Q, Zhao W-H, Hara Y, Shimamura T (2001) Epigallocatechin gallate synergy with ampicillin/sulbactam against 28 clinical isolates of methicillin-resistant Staphylococcus aureus. J Antimicrob Chemother 48:361–364CrossRefPubMedGoogle Scholar
  36. Häkkinen S, Kärenlampi S, Mykkänen H, Heinonen M, Törrönen R (2000) Ellagic acid-content in berries: influence of domestic processing and storage. Eur Food Res Technol 212:75–80CrossRefGoogle Scholar
  37. Häkkinen SH, Kärenlampi SO, Heinonen MI, Mykkänen HM, Törrönen RA (1999) Content of the flavonols quercetin, myricetin, and kaempferol in 25 edible berries. J Agric Food Chem 47:2274–2279CrossRefPubMedGoogle Scholar
  38. Ikigai H, Nakae T, Hara Y, Shimamura T (1993) Bactericidal catechins damage the lipid bilayer. Biochim Biophys Acta 1147:132–136PubMedGoogle Scholar
  39. Kolodzeij H, Kayser O, Latte KP (2003) Evaluation of the antimicrobial potency of tannins and related compounds using the microdilution broth method. Planta Med 65:444–446Google Scholar
  40. Kontiokari T, Laitinen J, Järvi L, Pokka T, Sundqvist K, Uhari M (2003) Dietary factors protecting women from urinary tract infection. Am J Clin Nutr 77:600–604PubMedGoogle Scholar
  41. Kubo I, Xiao P, Fujita K (2002) Anti-MRSA activity of alkyl gallates. Bioorg Med Chem Lett 12:113–116CrossRefPubMedGoogle Scholar
  42. Kubo I, Fujita K, Nihei K, Masuoka N (2003) Non-antibiotic antibacterial activity of dodecyl gallate. Bioorg Med Chem 11:573–580CrossRefPubMedGoogle Scholar
  43. Levy SB (2002) Active efflux, a common mechanisms for biocide and antibiotic resistance. J Appl Microbiol Symp Suppl 92:65S–71SGoogle Scholar
  44. Maillard JY (2002) Bacterial target sites for biocide action. J Appl Microbiol Symp [Suppl] 90:16S–27SGoogle Scholar
  45. Mazur WM, Uehara M, Wähälä K, Adlercreutz H (2000) Phyto-oestrogen content of berries, and plasma concentrations and urinary excretion of enterolactone after a single strawberry-meal in human subjects. Brit J Nutr 83:381–387PubMedGoogle Scholar
  46. Mullen W, Stewart AJ, Lean MEJ, Gardner P, Duthie GG, Crozier A (2002) Effect of freezing and storage on the phenolics, ellagitannins, flavonoids, and antioxidant capacity of red raspberries. J Agric Food Chem 50:5197–5201CrossRefPubMedGoogle Scholar
  47. Määttä K, Kamal-Eldin A, Törrönen R (2001) Phenolic compounds in berries of black, red, green, and white currants (Ribes sp.). Antioxid Redox Sign 3:981–993CrossRefGoogle Scholar
  48. Nanayakkara NP, Burandt CL Jr, Jacob MR (2002) Flavonoids with activity against methicillin-resistant Staphylococcus aureus from Dalea scandens var. paucifolia. Planta Med 68:519–522CrossRefPubMedGoogle Scholar
  49. Nikaido H (2003) Molecular basics of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev 64:593–656CrossRefGoogle Scholar
  50. Nogueira MCL, Oyarzábal OA, Gombas DE (2003) Inactivation of Escherichia coli O157:H7, Listeria monocytogenes, and Salmonella in cranberry, lemon, and lime juice concentrates. J Food Protect 66:1637–1641Google Scholar
  51. Ofek I, Goldhar J, Zafriri D, Lis H, Adar R, Sharon N (1991) Anti-Escherichia coli adhesin activity of cranberry and blueberry juices. NE J Med 324:1599Google Scholar
  52. Ow YY, Stupans I (2003) Gallic acid and gallic acid derivatives: effects on drug metabolizing enzymes. Curr Drug Metab 4:241–248PubMedGoogle Scholar
  53. Paulus W (1993) Microbicides for the protection of materials—a handbook. Chapman & Hall, London, p 496Google Scholar
  54. Poole K (2004) Efflux-mediated multiresistance in Gram-negative bacteria. Clin Microbiol Infect 10:12–26CrossRefGoogle Scholar
  55. Puupponen-Pimiä R, Nohynek L, Meier C, Kähkönen M, Heinonen M, Hopia A, Oksman-Caldentey K-M (2001) Antimicrobial properties of phenolic compounds from berries. J Appl Microbiol 90:494–507CrossRefPubMedGoogle Scholar
  56. Puupponen-Pimiä R, Aura A-M, Karppinen S, Oksman-Caldentey K-M, Poutanen K (2004a) Interactions between plant bioactive food ingredients and intestinal flora—effects on human health. Biosci Microflora 23:67–80Google Scholar
  57. Puupponen-Pimiä R, Nohynek L, Schmidlin S, Kähkönen M, Heinonen M, Määttä-Riihinen K, Oksman-Caldentey K-M (2004b) Berry phenolics selectively inhibit the growth of intestinal pathogens. J Appl Microbiol (in press)Google Scholar
  58. Rauha J-P, Remes S, Heinonen M, Hopia A, Kähkönen M, Kujala T, Pihlaja K, Vuorela H, Vuorela P (2000) Antimicrobial effects of Finnish plant extracts containing flavonoids and other phenolic compounds. Int J Food Microbiol 56:3–12CrossRefPubMedGoogle Scholar
  59. Reed J, Howell A, Cunningham D, Krueger C (2003) Differences in structure and bacterial anti-adhesion activity of cranberry proanthocyanidins compared to proanthocyanidins from other foods. Proceedings of the 1st International conference on polyphenols and health. 18–21 November 2003, Vichy, France. Poster abstract P28Google Scholar
  60. Reid G, Hsieh J, Potter P, Mighton J, Lam D, Warren D, Stephenson J (2001) Cranberry juice consumption may reduce biofilms on uroepithelial cells: Pilot study in spinal cord injured patients. Spinal Cord 39:26–30CrossRefPubMedGoogle Scholar
  61. Roccaro AS, Blanco AR, Giuliano F, Rusciano D, Enea V (2004) Epigallocatechin-gallate enhances the activity of tetracycline in staphylococci by inhibiting its efflux from bacterial cells. Antimicrob Agents Chemother 48:1968–1973CrossRefPubMedGoogle Scholar
  62. Ryan T, Wilkinson JM, Cavanagh HMA (2001) Antibacterial activity of raspberry cordial in vitro. Veter Sci 71:155–159CrossRefGoogle Scholar
  63. Scalbert A (1991) Antimicrobial properties of tannins. Phytochemistry 30:3875–3883CrossRefGoogle Scholar
  64. Sobota AE (1984) Inhibition of bacterial adherence by cranberry juice: potential use for the treatment of urinary tract infections. J Urol 131:1013–1016PubMedGoogle Scholar
  65. Stapleton PD, Shah S, Anderson JC, Hara Y, Hamilton-Miller JMT, Taylor PW (2004) Modulation of β-lactam resistance in Staphylococcus aureus by catechins and gallates. Int J Antimicrob Agents 23:462–467CrossRefPubMedGoogle Scholar
  66. Tanaka T, Tachibana H, Nonaka B, Nishioka I, Hsu F-L, Kohda H, Tanaka O (1993) Tannins and related compounds CXXII. New dimeric, trimeric and tetrameric ellagitannins, lambertianins A-D, from Rubus lambertianus SERINGE. Chem Pharm Bull 41:1214–1220PubMedGoogle Scholar
  67. Tegos G, Stermitz FR, Lomovskaya O, Lewis K (2002) Multidrug pump inhibitors uncover remarkable activity of plant antimicrobials. Antimicrob Agents Chemother 46:3133–3141CrossRefPubMedGoogle Scholar
  68. Toda M, Okubo S, Hiyoshi R, Shimamura T (1989) The bactericidal activity of tea and coffee. Lett Appl Microbiol 8:123–125Google Scholar
  69. Törrönen R, Häkkinen S, Kärenlampi S, Mykkänen H (1997) Flavonoids and phenolic acids in selected berries. Cancer Lett 114:191–192CrossRefPubMedGoogle Scholar
  70. Ulltveit G (1998) (Wild berries) Ville baer. Technologisk forlag, 2nd edn. NW Damm, Oslo, Norway, pp 1–166Google Scholar
  71. Ultee A, Bennik MHJ, Moezelaar R (2002) The phenolic hydroxyl group of carvacrol is essential for action against the food-borne pathogen Bacillus cereus. Appl Environ Microbiol 68:1561–1568CrossRefPubMedGoogle Scholar
  72. Vattem DA, Lin Y-T, Labbe RG, Shetty K (2003) Antimicrobial activity against select food-borne pathogens by phenolic antioxidants enriched in cranberry pomace by solid-state bioprocessing using the food grade fungus Rhizopus oligosporus. Process Biochem 39:1939–1946CrossRefGoogle Scholar
  73. Vattem DA, Shetty K (2003) Ellagic acid production and phenolic antioxidant activity in cranberry pomace (Vaccinium macrocarpon) mediated by Lentinus edodes using a solid-state system. Process Biochem 39:367–379CrossRefGoogle Scholar
  74. Vattem DA, Lin Y-T, Labbe RG, Shetty K (2004) Phenolic antioxidant mobilization in cranberry pomace by solid-state bioprocessing using food grade fungus Lentinus edodes and effect on antimicrobial activity against select food borne pathogens. Innovat Food Sci Emerg Technol 5:81–91CrossRefGoogle Scholar
  75. Viberg U, Sjöholm I (1996) Blåbär och lingon—bär med tradition och framtid (in Swedish). Livsmedesteknik 38:38–39Google Scholar
  76. Viljakainen S (2003) Reduction of acidity in northern region berry juices. PhD Thesis, Helsinki University of TechnologyGoogle Scholar
  77. Viljakainen S, Visti A, Laakso S (2002) Concentrations of organic acids and soluble sugars in juices from Nordic berries. Acta Agric Scand 52:101–109CrossRefGoogle Scholar
  78. Vivas N, Lonvaud-Funel A, Glories Y (1997) Effects of phenolic acids and anthocyanins on growth, viability and malolactic activity of a lactic acid bacterium. Food Microbiol 14:291–300CrossRefGoogle Scholar
  79. Vuorinen H, Määttä K, Törrönen R (2000) Content of the flavonols myricetin, quercetin, and kaempferol in Finnish berry wines. J Agric Food Chem 48:2675–2680CrossRefPubMedGoogle Scholar
  80. Walsh SE, Maillard JY, Russell AD, Catrenich CE, Charbonneau DL, Bartolo RG (2003) Activity and mechanisms of action of selected biocidal agents on Gram-positive and -negative bacteria. J Appl Microbiol 94:240–247CrossRefPubMedGoogle Scholar
  81. Weiss EI, Lev-Dor R, Sharon N, Ofek I (2002) Inhibitory effect of a high-molecular-weight constituent of cranberry on adhesion of oral bacteria. Crit Rev Food Sci Nutr 42 [Suppl]:285–292PubMedGoogle Scholar
  82. Wen A, Delaquis P, Stanich K, Toivonen P (2003) Antilisterial activity of selected phenolic acids. Food Microbiol 20:305–311CrossRefGoogle Scholar
  83. Zafriri D, Ofek I, Pocino AR, Sharon N (1989) Inhibitory activity of cranberry juice on adherence of type 1 and P fimbriated Escherichia coli to eucariotic cells. Antimicrob Agents Chemother 33:92–98PubMedGoogle Scholar
  84. Zhao W-H, Hu Z-Q, Hara Y, Shimamura T (2001a) Inhibition by epigallocatechin gallate (EGCg) of conjugative R plasmid transfer in Escherichia coli. J Infect Chemother 7:195–197CrossRefPubMedGoogle Scholar
  85. Zhao W-H, Hu Z-Q, Okubo S, Hara Y, Shimamura T (2001b) Mechanism of synergy between epigallacatechin gallate and β-lactams against methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 45:1737–1742CrossRefPubMedGoogle Scholar
  86. Zhao W-H, Asano N, Hu Z-Q, Shimamura T (2003) Restoration of antibacterial activity of β-lactams by epigallocatechin gallate against β-lactamase-producing species depending on location of β-lactamase. J Pharm Pharmacol 55:735–740CrossRefPubMedGoogle Scholar
  87. Zheng Z, Shetty K (1998) Cranberry processing waste for solid-state fungal inoculant production. Process Biochem 33:323–329CrossRefGoogle Scholar
  88. Zheng Z, Shetty K (2000) Solid-state bioconversion of phenolics from cranberry pomace and role of Letinus ododes beta-glucosidase. J Agric Food Chem 48:895–900CrossRefPubMedGoogle Scholar
  89. Yoda Y, Hu Z-Q, Zhao W-H (2004) Different susceptibilities of Staphylococcus and Gram-negative rods to epigallocatechin gallate. J Infect Chemother 10:55–58CrossRefPubMedGoogle Scholar

Copyright information

©  2004

Authors and Affiliations

  • Riitta Puupponen-Pimiä
    • 1
    Email author
  • Liisa Nohynek
    • 1
  • Hanna-Leena Alakomi
    • 1
  • Kirsi-Marja Oksman-Caldentey
    • 1
  1. 1.VTT BiotechnologyVTTFinland

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