Antimicrobial potential of polyphenols extracted from almond skins
G. Mandalari
Pharmaco-Biological Department, University of Messina, Viale Annunziata, Messina, Italy
Model Gut Platform, Institute of Food Research, Norwich Research Park, Norwich, UK
Search for more papers by this authorC. Bisignano
Pharmaco-Biological Department, University of Messina, Viale Annunziata, Messina, Italy
Search for more papers by this authorM. D’Arrigo
Pharmaco-Biological Department, University of Messina, Viale Annunziata, Messina, Italy
Search for more papers by this authorG. Ginestra
Pharmaco-Biological Department, University of Messina, Viale Annunziata, Messina, Italy
Search for more papers by this authorA. Arena
Department of Surgical Science, Unit of Microbiology, University of Messina, Messina, Italy
Search for more papers by this authorA. Tomaino
Pharmaco-Biological Department, University of Messina, Viale Annunziata, Messina, Italy
Search for more papers by this authorM.S.J. Wickham
Model Gut Platform, Institute of Food Research, Norwich Research Park, Norwich, UK
Search for more papers by this authorG. Mandalari
Pharmaco-Biological Department, University of Messina, Viale Annunziata, Messina, Italy
Model Gut Platform, Institute of Food Research, Norwich Research Park, Norwich, UK
Search for more papers by this authorC. Bisignano
Pharmaco-Biological Department, University of Messina, Viale Annunziata, Messina, Italy
Search for more papers by this authorM. D’Arrigo
Pharmaco-Biological Department, University of Messina, Viale Annunziata, Messina, Italy
Search for more papers by this authorG. Ginestra
Pharmaco-Biological Department, University of Messina, Viale Annunziata, Messina, Italy
Search for more papers by this authorA. Arena
Department of Surgical Science, Unit of Microbiology, University of Messina, Messina, Italy
Search for more papers by this authorA. Tomaino
Pharmaco-Biological Department, University of Messina, Viale Annunziata, Messina, Italy
Search for more papers by this authorM.S.J. Wickham
Model Gut Platform, Institute of Food Research, Norwich Research Park, Norwich, UK
Search for more papers by this authorAbstract
Aims: To evaluate the antimicrobial properties of flavonoid-rich fractions derived from natural and blanched almond skins, the latter being a by-product from the almond processing industry.
Methods and Results: Almond skin extracts were tested against Gram-negative bacteria (Escherichia coli, Pseudomonas aeruginosa, Salmonella enterica, Serratia marcescens), Gram-positive bacteria (Listeria monocytogenes, Enterococcus hirae, Staphylococcus aureus, Enterococcus durans) and the yeast Candida albicans. Almond skin fractions were found to have antimicrobial activity against L. monocytogenes and Staph. aureus in the range 250–500 μg ml−1, natural skins showing antimicrobial potential against the Gram-negative Salm. enterica. The interactions between three almond skin flavonoids were also evaluated with isobolograms.
Conclusions: Pairwise combinations of protocatechuic acid, naringenin and epicatechin showed both synergistic and indifferent interactions against Salm. enterica and Staph. aureus. Antagonism was observed against L. monocytogenes with all combinations tested. Further studies need to be performed to understand the mechanisms responsible for these interactions.
Significance and Impact of the Study: Almond skins are a potential source of natural antimicrobials.
References
- Bae, E.A., Han, M.J. and Kim, D.H. (1999) In vitro anti-Helicobacter pylori activity of some flavonoids and their metabolites. Planta Med 65, 442–443.
- Benavente-Garcia, O., Castillo, J., Marin, F.R., Ortuno, A. and Del Rio, J.A. (1997) Uses and properties of Citrus flavonoids. J Agric Food Chem 45, 4505–4515.
- Beuchat, L.R. and Golden, D.A. (1989) Antimicrobials occurring naturally in foods. Food Technol 43, 134–142.
- Clinical and Laboratory Standards Institute, M100-S18 (2008) Performance Standards for Antimicrobial Susceptibility Testing, Seventeenth Informational Supplement Clinical Laboratory Standards Institute, Wayne, PA.
- D’Arrigo, M, Ginestra, G., Mandalari, G., Furneri, P.M. and Bisignano, G. (2010) Synergism and postantibiotic effect of tobramycin and Melaleuca alternifolia (tea tree) oil against Staphylococcus aureus and Escherichia coli. Phytomedicine 17, 317–322.
- Davidson, P.M. and Parish, M.E. (1989) Methods for testing the efficacy of food antimicrobials. Food Technol 43, 148–155.
- Espin, J.C., Garcia-Conesa, M.T. and Tomas-Barberan, F.A. (2007) Nutraceuricals: facts and fiction. Phytochemistry 68, 2986–3008.
- Funatogawa, K., Hayashi, S., Shimomura, H., Yoshida, T., Hatano, T., Ito, H. and Hirai, Y. (2004) Antibacterial activity of hydrolysable tannins derived from medicinal plants against Helicobacter pylori. Microbiol Immunol 48, 251–261.
- Gonzáles, J.F., Gañán, J., Ramiro, A., Gonzáles-García, C.M., Encinar, J.M., Sabio, E. and Román, S. (2006) Almond residues gasification plant for generation of electric power. Preliminary study. Fuel Proc Technol 87, 149–155.
-
Gould, G.W. (1996) Industry perspectives on the use of natural antimicrobials and inhibitors for food applications.
J Food Protec
59 (3, Suppl.), 82–86.
10.4315/0362-028X-59.13.82 Google Scholar
- Grasser, L.A., Fadel, J.O., Garnett, I. and DePeters, E.J. (1995) Quantity and economic importance of nine selected by-products. J Dairy Sci 78, 962–971.
- Hammer, K.A., Carson, C.F. and Riley, T.V. (1999) Antimicrobial activity of essential oils and other plant extracts. J Appl Microbiol 86, 985–990.
- Hwang, D.R., Tsai, Y.C., Lee, J.C., Huang, K.K., Lin, R.K., Ho, C.H., Chiou, J.M., Lin, Y.T. et al. (2004) Inhibition of hepatitis C virus replication by arsenic trioxide. Antimicrob Agents Chemother 48, 2876–2882.
- Jenner, A.M., Rafter, J. and Halliwell, B. (2005) Human fecal water content of phenolics: the extent of colonic exposure to aromatic compounds. Free Rad Biol Med 38, 763–772.
- Knekt, P., Kumpulainen, J., Jarvinen, R., Rissanen, H., Heliovaara, M., Reunanen, A., Hakulinen, T. and Aromaa, A. (2002) Flavonoid intake and risk of chronic diseases. Am J Clin Nutr 76, 560–568.
- Ku, K.-J., Hong, Y.-H. and Song, K.B. (2008) Mechanical properties of a Gelidium corneum edible film containing catechin and its application in sausages. Food Chem 73, C217–C221.
- Lee, Y.-S., Kang, O.-H., Choi, J.-G., Oh, Y.-C., Chae, H.-S., Kim, J.H., Park, H., Sohn, D. H. et al. (2008) Synergistic effects of the combination of galancin with gentamicin against methicillin-resistant Staphylococcus aureus. J Microbiol 46, 283–288.
- Lis-Balchim, M. and Deans, S.G. (1997) Bioactivity of selected plant essential oils against Listeria monocytogenes. J Appl Bacteriol 82, 759–762.
- Liu, R.H. (2004) Potential synergy of phytochemicals in cancer prevention: mechanism of action. J Nutr 134, 3479S–3485S.
- Mabe, K., Yamada, M., Oguni, I. and Takahashi, T. (1999) In vitro and in vivo activities of tea catechins against Helicobacter pylori. Antimicrob Agents Chemother 43, 1788–1791.
- Manach, C. and Donovan, J.L. (2004) Pharmacokinetics and metabolism of dietary flavonoids in humans. Free Rad Res 38, 771–785.
- Mandalari, G., Bennett, R.N., Bisignano, G., Trombetta, D., Saija, A., Faulds, C.B., Gasson, M.J. and Narbad, A. (2007) Antimicrobial activity of flavonoids extracted from bergamot (Citrus bergamia Risso) peel, a byproduct of the essential oil industry. J Appl Microbiol 103, 2056–2064.
- Mandalari, G., Faulks, R.M., Rich, G.T., Lo Turco, V., Picout, D.R., Lo Curto, R.B., Bisignano, G., Dugo, P. et al. (2008) Release of protein, lipid and vitamin E from almond seeds during digestion. J Agric Food Chem 56, 3409–3416.
- Mandalari, G., Tomaino, A., Arcoraci, T., Martorana, M., Lo Turco, V., Cacciola, F., Rich, G.T., Bisignano, C. et al. (2010a) Characterization of polyphenols, lipids and dietary fibre from skins of almonds (Amygdalus communis L.). J Food Comp Anal 23, 166–174.
- Mandalari, G., Tomaino, A., Rich, G.T., Lo Curto, R.B., Arcoraci, T., Martorana, M., Bisignano, C., Saija, A. et al. (2010b) Polyphenol and nutrient release from skin of almonds during simulated human digestion. Food Chem 122, 1083–1088.
- Martini, S., D’Addario, C., Colavevich, A., Focardi, S., Borghini, F., Santucci, A., Figura, N. and Rossi, C. (2009) Antimicrobial activity against Helicobacter pylori strains and antioxidant properties of blackberry leaves (Rubus ulmifolius) and isolated compounds. Int J Antimicrob Ag 34, 50–59.
- Olasupo, N.A., Fitzgerald, D.J., Narbad, A. and Gasson, M.J. (2004) Inhibition of Bacillus subtilis and Listeria innocua by nisin in combination with some naturally occurring organic compounds. J Food Protect 67, 596–600.
- Puupponen-Pimiä, R., Nohynek, L., Meier, C., Kähkönen, M., Heinonen, M., Hopia, A. and Oksman-Caldentey, K-M. (2001) Antimicrobial properties of phenolic compounds in berries. J Appl Microbiol 90, 494–507.
- Puupponen-Pimiä, R., Nohynek, L., Alakomi, H.L. and Oksman-Caldentey, K-M. (2006) The action of berry phenolics against human intestinal pathogens. Biofactors 23, 243–251.
- Rechner, A.R., Smtih, M.A., Kuhnle, G., Gibson, G.R., Debnam, E.S., Srai, S.K.S., Moore, K.P. and Rice-Evans, C.A. (2004) Colonic metabolism of dietary polyphenols: influence of structure on microbial fermentation products. Free Rad Biol Med 36, 212–225.
- Rios, L. Y., Gonthier, M.-P., Remesy, C., Mila, I., Lapierre, C., Lazarus, S.A., Williamson, G. and Scalbert, A. (2003) Chocolate intake increases excretion of polyphenol-derived phenolic acids in healthy human subjects. Am J Clin Nutr 77, 912–918.
- Sabate, J., Haddad, E., Tanzman, J.S., Jambazian, P. and Rajaram, S. (2003) Serum lipid response to the graduated enrichment of a Step I diet with almonds: a randomized feeding trial. Am J Clin Nutr 77, 1379–84.
- Scalbert, A. (1991) Antimicrobial properties of tannins. Phytochemistry 12, 3875–3883.
- Sikkema, J.J., De Bont, A.M. and Poolman, B. (1994) Interactions of cyclic hydrocarbons with biological membranes. J Biolog Chem 269, 8022–8028.
- Simons, A.L., Renouf, M., Hendrich, S. and Murphy, P.A. (2005) Human gut microbial degradation of flavonoids: structure–function relationships. J Agric Food Chem 53, 4258–4263.
- Taguri, T., Tanaka, T. and Kouno, I. (2004) Antimicrobial activity of 10 different plant polyphenols against bacteria causing food-borne disease. Biologic and Pharmac Bulletin 27, 1965–1969.
- Tombola, F., Campello, S., De Luca, L., Ruggiero, P., Del Giudice, G., Papini, E. and Zoratti, M. (2003) Plant polyphenols inhibit VacA, a toxin secreted by the gastric pathogen Helicobacter pylori. FEBS Lett 543, 184–189.
- Visalli, M.A., Jacobs, M.R. and Appelbaum, P.C. (1998) Determination of activities of levofloxacin, alone and combined with gentamicin, ceftazidime, cefpirome, and meropenem, against 124 strains of Pseudomonas aeruginosa by checkerboard and time-kill methodology. Antimicrob Agents Chemother 42, 953–955.
- Vuorela, S., Kreander, K., Karonen, M., Nieminen, R., Hämäläinen, M., Galkin, A., Laitinen, L., Salminen, E.M. et al. (2005) Preclinical evaluation of rapeseed, raspberry, and pine bark phenolics for health related effects. J Agric Food Chem 53, 5922–5931.
- White, R.L., Burgess, D.S., Manduru, M. and Bosso, J.A. (1996) Comparison of three different in vitro methods of detecting synergy: time-kill, checkerboard, and E test. Antimicrob Ag Chemother 40, 1914–1918.
