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References

  1. Alvarez M, Tran JH, Chow N, Jacoby GA. 2004. Epidemiology of conjugative plasmid-mediated AmpC betalactamases in the United States. Antimicrob. Agents Chemother. 48: 533-537.
    Pubmed PMC CrossRef
  2. Bajpai VK, Sharma A, Baek KH. 2013. Antibacterial mode of action of Cudrania tricuspidata fruit essential oil, affecting membrane permeability and surface characteristics of foodborne pathogens. Food Control 32: 582-590.
    CrossRef
  3. Becerril R, Gomez-Lus R, Goni P, Lopez P, Nerin C. 2007. Combination of analytical and microbiological techniques to study the antimicrobial activity of a new active food packaging containing cinnamon or oregano against E. coli and S. aureus. Anal. Bioanal. Chem. 388: 1003-1011.
    Pubmed CrossRef
  4. Bolla JM, Alibert-Franco S, Handzlik J, Chevalier J, Mahamoud A, Boyer G, et al. 2011. Strategies for bypassing the membrane barrier in multidrug resistant gram-negative bacteria. FEBS Lett. 585: 1682-1690.
    Pubmed CrossRef
  5. Borges A, Ferreira C, Saavedra MJ, Simoes M. 2013. Antibacterial activity and mode of action of ferulic and gallic acids against pathogenic bacteria. Microb. Drug Resist. 19: 256-265.
    Pubmed CrossRef
  6. Burt SA, Reinders RD. 2003. Antibacterial activity of selected plant essential oils against Escherichia coli O157:H7. Lett. Appl. Microbiol. 36: 162-167.
    Pubmed CrossRef
  7. Carson CF, Mee BJ, Riley TV. 2002. Mechanism of action of Melaleuca alternifolia (tea tree) oil on Staphylococcus aureus determined by time-kill, lysis, leakage, and salt tolerance assays and electron microscopy. Antimicrob. Agents Chemother. 46: 1914-1920.
    Pubmed PMC CrossRef
  8. Cho YS, Oh JJ, Oh KH. 2011. Synergistic anti-bacterial and proteomic effects of epigallocatechin gallate on clinical isolates of imipenem-resistant Klebsiella pneumoniae. Phytomedicine 18:941-946.
    Pubmed CrossRef
  9. Devi KP, Sakthivel R, Nisha SA, Suganthy N, Pandian SK. 2012. Eugenol alters the integrity of cell membrane and acts against the nosocomial pathogen Proteus mirabilis. Arch. Pharm. Res. 36: 282-292.
    Pubmed CrossRef
  10. Eumkeb G, Siriwong S, Phitaktim S, Rojtinnakorn N, Sakdarat S. 2012. Synergistic activity and mode of action of flavonoids isolated from smaller galangal and amoxicillin combinations against amoxicillin-resistant Escherichia coli. J. Appl. Microbiol. 112: 55-64.
    Pubmed CrossRef
  11. Eumkeb G, Siriwong S, Thumanu K. 2012. Synergistic activity of luteolin and amoxicillin combination against amoxicillinresistant Escherichia coli and mode of action. J. Photochem. Photobiol. B Biol. 117: 247-253.
  12. Georgopapadakou NH. 1993. Penicillin-binding proteins and bacterial resistance to beta-lactams. Antimicrob. Agents Chemother. 37: 2045-2053.
    Pubmed PMC CrossRef
  13. Gilbert P, Evans DJ, Evans E, Duguid IG, Brown MR. 1991. Surface characteristics and adhesion of Escherichia coli and Staphylococcus epidermidis. J. Appl. Bacteriol. 71: 72-77.
    Pubmed CrossRef
  14. Goni P, Lopez P, Sanchez C, Gomez-Lus R, Becerril R, Nerin C. 2009. Antimicrobial activity in the vapour phase of a combination of cinnamon and clove essential oils. Food Chem. 116: 982-989.
    CrossRef
  15. Hemaiswarya S, Doble M. 2009. Synergistic interaction of eugenol with antibiotics against gram-negative bacteria. Phytomedicine 16: 997-1005.
    Pubmed CrossRef
  16. Kojima S, Nikaido H. 2013. Permeation rates of penicillins indicate that Escherichia coli porins function principally as nonspecific channels. Proc. Natl. Acad. Sci. USA 110: E2629-E2634.
    Pubmed PMC CrossRef
  17. Li Y-Q, Kong D-X, Wu H. 2013. Analysis and evaluation of essential oil components of cinnamon barks using GC–MS and FTIR spectroscopy. Ind. Crops Prod. 41: 269-278.
    CrossRef
  18. Livermore DM. 1996. Are all beta-lactams created equal? Scand. J. Infect. Dis. 101: 33-43.
  19. Lorian V (ed.) 2005. Antibiotics in Laboratory Medicine, pp. 365-405. 5th Ed. Lippincott Williams & Wilkins.
  20. Macheboeuf P, Contreras-Martel C, Job V, Dideberg O, Dessen A. 2006. Penicillin binding proteins: key players in bacterial cell cycle and drug resistance processes. FEMS Microbiol. Rev. 30: 673-691.
    Pubmed CrossRef
  21. Mahadlek J, Charoenteeraboon J, Phaechamud T. 2012. Combination effects of the antimicrobial agents and cinnamon oil. Adv. Mater. Res. 506: 246-249.
    CrossRef
  22. Marri L, Dallai R, Marchini D. 1996. The novel antibacterial peptide ceratotoxin A alters permeability of the inner and outer membrane of Escherichia coli K-12. Curr. Microbiol. 33: 40-43.
    Pubmed CrossRef
  23. Nazari M, Kurdi M, Heerklotz H. 2012. Classifying surfactants with respect to their effect on lipid membrane order. Biophys. J. 102: 498-506.
    Pubmed PMC CrossRef
  24. Obst S, Kastowsky M, Bradaczek H. 1997. Molecular dynamics simulations of six different fully hydrated monomeric conformers of Escherichia coli re-lipopolysaccharide in the presence and absence of Ca2+. Biophys. J. 72: 1031-1046.
    CrossRef
  25. Palmer J, Flint S, Brooks J. 2007. Bacterial cell attachment, the beginning of a biofilm. J. Ind. Microbiol. Biotechnol. 34:577-588.
    Pubmed CrossRef
  26. Paul S, Dubey RC, Maheswari DK, Kang SC. 2011. Trachyspermum ammi (L.) fruit essential oil influencing on membrane permeability and surface characteristics in inhibiting food-borne pathogens. Food Control 22: 725-731.
    CrossRef
  27. Pina-Pérez MC, Martínez-López A, Rodrigo D. 2012. Cinnamon antimicrobial effect against Salmonella typhimurium cells treated by pulsed electric fields (PEF) in pasteurized skim milk beverage. Food Res. Int. 48: 777-783.
    CrossRef
  28. Sharma A, Bajpai VK, Baek KH. 2013. Determination of antibacterial mode of action of Allium sativum essential oil against foodborne pathogens using membrane permeability and surface characteristic parameters. J. Food Saf. 33: 197-208.
    CrossRef
  29. Sikkema J, de Bont JA, Poolman B. 1995. Mechanisms of membrane toxicity of hydrocarbons. Microbiol. Rev. 59: 201-222.
    Pubmed PMC
  30. Tymczyszyn EE, del Rosario Diaz M, Gomez-Zavaglia A, Disalvo EA. 2007. Volume recovery, surface properties and membrane integrity of Lactobacillus delbrueckii subsp. bulgaricus dehydrated in the presence of trehalose or sucrose. J. Appl. Microbiol. 103: 2410-2419.
    Pubmed CrossRef
  31. Vaara M. 1992. Agents that increase the permeability of the outer membrane. Microbiol. Rev. 56: 395-411.
    Pubmed PMC
  32. van der Mei HC, de Vries J, Busscher HJ. 1993. Hydrophobic and electrostatic cell surface properties of thermophilic dairy streptococci. Appl. Environ. Microbiol. 59: 4305-4312.
    Pubmed PMC
  33. Walsh C. 2000. Molecular mechanisms that confer antibacterial drug resistance. Nature 406: 775-781.
    Pubmed CrossRef
  34. Winson MK, Swift S, Fish L, Throup JP, Jorgensen F, Chhabra SR, et al. 1998. Construction and analysis of luxCDABE-based plasmid sensors for investigating N-acyl homoserine lactone-mediated quorum sensing. FEMS Microbiol. Lett. 163: 185-192.
    Pubmed CrossRef
  35. Winzer K, Falconer C, Garber NC, Diggle SP, Camara M, Williams P. 2000. The Pseudomonas aeruginosa lectins PA-IL and PA-IIL are controlled by quorum sensing and by RpoS. J. Bacteriol. 182: 6401-6411.
    Pubmed PMC CrossRef
  36. Woldringh CL, van Iterson W. 1972. Effects of treatment with sodium dodecyl sulfate on the ultrastructure of Escherichia coli. J. Bacteriol. 111: 801-813.
    Pubmed PMC
  37. Yap PSX, Lim SH, Hu CP, Yiap BC. 2013. Combination of essential oils and antibiotics reduce antibiotic resistance in plasmid-conferred multidrug resistant bacteria. Phytomedicine 20: 710-713.
    Pubmed CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2015; 25(8): 1299-1306

Published online August 28, 2015 https://doi.org/10.4014/jmb.1407.07054

Copyright © The Korean Society for Microbiology and Biotechnology.

Antibacterial Mode of Action of Cinnamomum verum Bark Essential Oil, Alone and in Combination with Piperacillin, Against a Multi-Drug-Resistant Escherichia coli Strain

Polly Soo Xi Yap 1, Thiba Krishnan 2, Kok-Gan Chan 2 and Swee Hua Erin Lim 3*

1School of Postgraduate Studies and Research, International Medical University, 57000 Kuala Lumpur, Malaysia, 2Division of Genetics and Molecular Biology, Institute of Biological Sciences, Faculty of Science, University of Malaya, 50603 Kuala Lumpur, Malaysia, 3Department of Physiology, Perdana University-Royal College of Surgeons Ireland (PU-RCSI), 43400 Serdang, Selangor, Malaysia

Received: July 21, 2014; Accepted: November 9, 2014

Abstract

This study aimed to investigate the mechanism of action of the cinnamon bark essential oil
(CB), when used singly and also in combination with piperacillin, for its antimicrobial and
synergistic activity against beta-lactamase TEM-1 plasmid-conferred Escherichia coli J53 R1.
Viable count of this combination showed a complete killing profile at 20 h and further
confirmed its synergistic effect by reducing the bacteria cell numbers. Analysis on the stability
of treated cultures for cell membrane permeability by CB when tested against sodium dodecyl
sulfate revealed that the bacterial cell membrane was disrupted by the essential oils. Scanning
electron microscopy observation and bacterial surface charge measurement also revealed that
CB causes irreversible membrane damage and reduces the bacterial surface charge. In
addition, bioluminescence expression of Escherichia coli [pSB1075] and E. coli [pSB401] by CB
showed reduction, indicating the possibility of the presence of quorum sensing (QS)
inhibitors. Gas-chromatography and mass spectrometry of the essential oil of Cinnamomum
verum showed that trans-cinnamaldehyde (72.81%), benzyl alcohol (12.5%), and eugenol
(6.57%) were the major components in the essential oil. From this study, CB has the potential
to reverse E. coli J53 R1 resistance to piperacillin through two pathways; modification in the
permeability of the outer membrane or bacterial QS inhibition.

Keywords: Cinnamomum verum, essential oil, chemical composition, antibacterial activity, membrane permeability, quorum sensing

References

  1. Alvarez M, Tran JH, Chow N, Jacoby GA. 2004. Epidemiology of conjugative plasmid-mediated AmpC betalactamases in the United States. Antimicrob. Agents Chemother. 48: 533-537.
    Pubmed KoreaMed CrossRef
  2. Bajpai VK, Sharma A, Baek KH. 2013. Antibacterial mode of action of Cudrania tricuspidata fruit essential oil, affecting membrane permeability and surface characteristics of foodborne pathogens. Food Control 32: 582-590.
    CrossRef
  3. Becerril R, Gomez-Lus R, Goni P, Lopez P, Nerin C. 2007. Combination of analytical and microbiological techniques to study the antimicrobial activity of a new active food packaging containing cinnamon or oregano against E. coli and S. aureus. Anal. Bioanal. Chem. 388: 1003-1011.
    Pubmed CrossRef
  4. Bolla JM, Alibert-Franco S, Handzlik J, Chevalier J, Mahamoud A, Boyer G, et al. 2011. Strategies for bypassing the membrane barrier in multidrug resistant gram-negative bacteria. FEBS Lett. 585: 1682-1690.
    Pubmed CrossRef
  5. Borges A, Ferreira C, Saavedra MJ, Simoes M. 2013. Antibacterial activity and mode of action of ferulic and gallic acids against pathogenic bacteria. Microb. Drug Resist. 19: 256-265.
    Pubmed CrossRef
  6. Burt SA, Reinders RD. 2003. Antibacterial activity of selected plant essential oils against Escherichia coli O157:H7. Lett. Appl. Microbiol. 36: 162-167.
    Pubmed CrossRef
  7. Carson CF, Mee BJ, Riley TV. 2002. Mechanism of action of Melaleuca alternifolia (tea tree) oil on Staphylococcus aureus determined by time-kill, lysis, leakage, and salt tolerance assays and electron microscopy. Antimicrob. Agents Chemother. 46: 1914-1920.
    Pubmed KoreaMed CrossRef
  8. Cho YS, Oh JJ, Oh KH. 2011. Synergistic anti-bacterial and proteomic effects of epigallocatechin gallate on clinical isolates of imipenem-resistant Klebsiella pneumoniae. Phytomedicine 18:941-946.
    Pubmed CrossRef
  9. Devi KP, Sakthivel R, Nisha SA, Suganthy N, Pandian SK. 2012. Eugenol alters the integrity of cell membrane and acts against the nosocomial pathogen Proteus mirabilis. Arch. Pharm. Res. 36: 282-292.
    Pubmed CrossRef
  10. Eumkeb G, Siriwong S, Phitaktim S, Rojtinnakorn N, Sakdarat S. 2012. Synergistic activity and mode of action of flavonoids isolated from smaller galangal and amoxicillin combinations against amoxicillin-resistant Escherichia coli. J. Appl. Microbiol. 112: 55-64.
    Pubmed CrossRef
  11. Eumkeb G, Siriwong S, Thumanu K. 2012. Synergistic activity of luteolin and amoxicillin combination against amoxicillinresistant Escherichia coli and mode of action. J. Photochem. Photobiol. B Biol. 117: 247-253.
  12. Georgopapadakou NH. 1993. Penicillin-binding proteins and bacterial resistance to beta-lactams. Antimicrob. Agents Chemother. 37: 2045-2053.
    Pubmed KoreaMed CrossRef
  13. Gilbert P, Evans DJ, Evans E, Duguid IG, Brown MR. 1991. Surface characteristics and adhesion of Escherichia coli and Staphylococcus epidermidis. J. Appl. Bacteriol. 71: 72-77.
    Pubmed CrossRef
  14. Goni P, Lopez P, Sanchez C, Gomez-Lus R, Becerril R, Nerin C. 2009. Antimicrobial activity in the vapour phase of a combination of cinnamon and clove essential oils. Food Chem. 116: 982-989.
    CrossRef
  15. Hemaiswarya S, Doble M. 2009. Synergistic interaction of eugenol with antibiotics against gram-negative bacteria. Phytomedicine 16: 997-1005.
    Pubmed CrossRef
  16. Kojima S, Nikaido H. 2013. Permeation rates of penicillins indicate that Escherichia coli porins function principally as nonspecific channels. Proc. Natl. Acad. Sci. USA 110: E2629-E2634.
    Pubmed KoreaMed CrossRef
  17. Li Y-Q, Kong D-X, Wu H. 2013. Analysis and evaluation of essential oil components of cinnamon barks using GC–MS and FTIR spectroscopy. Ind. Crops Prod. 41: 269-278.
    CrossRef
  18. Livermore DM. 1996. Are all beta-lactams created equal? Scand. J. Infect. Dis. 101: 33-43.
  19. Lorian V (ed.) 2005. Antibiotics in Laboratory Medicine, pp. 365-405. 5th Ed. Lippincott Williams & Wilkins.
  20. Macheboeuf P, Contreras-Martel C, Job V, Dideberg O, Dessen A. 2006. Penicillin binding proteins: key players in bacterial cell cycle and drug resistance processes. FEMS Microbiol. Rev. 30: 673-691.
    Pubmed CrossRef
  21. Mahadlek J, Charoenteeraboon J, Phaechamud T. 2012. Combination effects of the antimicrobial agents and cinnamon oil. Adv. Mater. Res. 506: 246-249.
    CrossRef
  22. Marri L, Dallai R, Marchini D. 1996. The novel antibacterial peptide ceratotoxin A alters permeability of the inner and outer membrane of Escherichia coli K-12. Curr. Microbiol. 33: 40-43.
    Pubmed CrossRef
  23. Nazari M, Kurdi M, Heerklotz H. 2012. Classifying surfactants with respect to their effect on lipid membrane order. Biophys. J. 102: 498-506.
    Pubmed KoreaMed CrossRef
  24. Obst S, Kastowsky M, Bradaczek H. 1997. Molecular dynamics simulations of six different fully hydrated monomeric conformers of Escherichia coli re-lipopolysaccharide in the presence and absence of Ca2+. Biophys. J. 72: 1031-1046.
    CrossRef
  25. Palmer J, Flint S, Brooks J. 2007. Bacterial cell attachment, the beginning of a biofilm. J. Ind. Microbiol. Biotechnol. 34:577-588.
    Pubmed CrossRef
  26. Paul S, Dubey RC, Maheswari DK, Kang SC. 2011. Trachyspermum ammi (L.) fruit essential oil influencing on membrane permeability and surface characteristics in inhibiting food-borne pathogens. Food Control 22: 725-731.
    CrossRef
  27. Pina-Pérez MC, Martínez-López A, Rodrigo D. 2012. Cinnamon antimicrobial effect against Salmonella typhimurium cells treated by pulsed electric fields (PEF) in pasteurized skim milk beverage. Food Res. Int. 48: 777-783.
    CrossRef
  28. Sharma A, Bajpai VK, Baek KH. 2013. Determination of antibacterial mode of action of Allium sativum essential oil against foodborne pathogens using membrane permeability and surface characteristic parameters. J. Food Saf. 33: 197-208.
    CrossRef
  29. Sikkema J, de Bont JA, Poolman B. 1995. Mechanisms of membrane toxicity of hydrocarbons. Microbiol. Rev. 59: 201-222.
    Pubmed KoreaMed
  30. Tymczyszyn EE, del Rosario Diaz M, Gomez-Zavaglia A, Disalvo EA. 2007. Volume recovery, surface properties and membrane integrity of Lactobacillus delbrueckii subsp. bulgaricus dehydrated in the presence of trehalose or sucrose. J. Appl. Microbiol. 103: 2410-2419.
    Pubmed CrossRef
  31. Vaara M. 1992. Agents that increase the permeability of the outer membrane. Microbiol. Rev. 56: 395-411.
    Pubmed KoreaMed
  32. van der Mei HC, de Vries J, Busscher HJ. 1993. Hydrophobic and electrostatic cell surface properties of thermophilic dairy streptococci. Appl. Environ. Microbiol. 59: 4305-4312.
    Pubmed KoreaMed
  33. Walsh C. 2000. Molecular mechanisms that confer antibacterial drug resistance. Nature 406: 775-781.
    Pubmed CrossRef
  34. Winson MK, Swift S, Fish L, Throup JP, Jorgensen F, Chhabra SR, et al. 1998. Construction and analysis of luxCDABE-based plasmid sensors for investigating N-acyl homoserine lactone-mediated quorum sensing. FEMS Microbiol. Lett. 163: 185-192.
    Pubmed CrossRef
  35. Winzer K, Falconer C, Garber NC, Diggle SP, Camara M, Williams P. 2000. The Pseudomonas aeruginosa lectins PA-IL and PA-IIL are controlled by quorum sensing and by RpoS. J. Bacteriol. 182: 6401-6411.
    Pubmed KoreaMed CrossRef
  36. Woldringh CL, van Iterson W. 1972. Effects of treatment with sodium dodecyl sulfate on the ultrastructure of Escherichia coli. J. Bacteriol. 111: 801-813.
    Pubmed KoreaMed
  37. Yap PSX, Lim SH, Hu CP, Yiap BC. 2013. Combination of essential oils and antibiotics reduce antibiotic resistance in plasmid-conferred multidrug resistant bacteria. Phytomedicine 20: 710-713.
    Pubmed CrossRef