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Cellular effects induced by Inula graveolens and Santolina corsica essential oils on Staphylococcus aureus | SpringerLink

Cellular effects induced by Inula graveolens and Santolina corsica essential oils on Staphylococcus aureus

Abstract

This study was conducted to evaluate the antibacterial activity of Inula graveolens and Santolina corsica essential oils on Staphylococcus aureus and investigate their effects at the cellular level. The mode of inhibition of both essential oils against S. aureus ATCC 6538P (CIP 53.156) was assessed by determining the minimum inhibitory concentration (MIC) and the minimum bactericidal concentration (MBC). The effects of time and treatment dose on cell viability were determined by time-kill and bacteriolysis assays. Marked structural changes were observed by transmission electron microscopy (TEM). A bactericidal mode of inhibition was established for both essential oils, which rapidly reduced the cell viability of S. aureus at their MIC (5 mg·ml-1). No lysis occurred after treatments with the MIC and eight times the MIC of each essential oil. Invaginations of the plasmic membrane with thickenings of the cell wall as well as an aggregation of the cytoplasmic contents were observed in S. aureus cells treated with the MIC of both essential oils. These results suggest that the cytoplasmic membrane and the cell wall are involved in the toxic action of Inula graveolens and Santolina corsica essential oils.

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References

  1. 1.

    National Nosocomial Infections Surveillance System (2004) National Nosocomial Infections Surveillance (NNIS) System Report, data summary from January 1992 through June 2004, issued October 2004. Am J Infect Control 32:470–485

    Article  Google Scholar 

  2. 2.

    CDC (2002) Staphylococcus aureus resistant to vancomycin—United States. JAMA 7:824–825

    Google Scholar 

  3. 3.

    Jevitt LA, Smith AJ, Williams PP, Raney PM, McGowan GE Jr, Tenover FC, Brown SD (2003) In vitro activities of daptomycin, linezolid, and quinupristin-dalfopristin against a challenge panel of staphylococci and enterococci, including vancomycin-intermediate Staphylococcus aureus and vancomycin-resistant Enterococcus faecium. Microb Drug Resist 9:389–393

    Article  CAS  PubMed  Google Scholar 

  4. 4.

    Tenover FC, Weigel LM, Appelbaum PC, McDougal LK, Chaitram J, McAllister S, Clark N, Killgore G, O’Hara CM, Jevitt L, Patel JB, Bozdogan B (2004) Vancomycin-resistant Staphylococcus aureus isolate from a patient in Pennsylvania. Antimicrob Agents Chemother 48:275–280

    Article  CAS  PubMed  Google Scholar 

  5. 5.

    Jacobson LM, Milstone AM, Zenilman J, Carroll KC, Arav-Boger R (2009) Daptomycin therapy failure in an adolescent with methicillin resistant Staphylococcus aureus bacteremia. Pediatr Infect Dis J 28:445–447

    Article  PubMed  Google Scholar 

  6. 6.

    Đordević S, Petrović S, Dobrić S, Milenković M, Vučićević D, Žižić S, Kukić J (2007) Antimicrobial, anti-inflammatory, anti-ulcer and anti-oxidant activities of Carlina acanthifolia root essential oil. J Ethnopharmacol 109:458–463

    Article  PubMed  Google Scholar 

  7. 7.

    De Sousa AC, Alviano DS, Blank AF, Alves PB, Alviano CS, Gattass CR (2004) Melissa officinalis L. essential oil: antitumoral and antioxidant activities. J Pharm Pharmacol 56:677–681

    Article  PubMed  Google Scholar 

  8. 8.

    Kumar A, Malik F, Bhushan S, Sethi VK, Shahi AK, Kaur J, Taneja SC, Qazi GN, Singh J (2008) An essential oil and its major constituent isointermedeol induce apoptosis by increased expression of mitochondrial cytochrome c and apical death receptors in human leukaemia HL-60 cells. Chem Biol Interact 171:332–337

    Article  CAS  PubMed  Google Scholar 

  9. 9.

    Xiao Y, Yang FQ, Li SP, Hu G, Lee SMY, Wang YT (2008) Essential oil of Curcuma wenyujin induces apoptosis in human hepatoma cells. World J Gastroenterol 14:4309–4318

    Article  PubMed  Google Scholar 

  10. 10.

    Jasicka-Misiak I, Lipok J, Nowakowska EM, Wieczorek PP, Mlynarz P, Kafarski P (2004) Antifungal activity of the carrot seed oil and its major sesquiterpene compounds. Z Naturforsch C 59:791–796

    CAS  PubMed  Google Scholar 

  11. 11.

    Pinto E, Pina-Vaz C, Salgueiro L, Gonçalves MJ, Costa-de-Oliviera S, Cavaleiro C, Palmeira A, Rodriguez A, Martinez-de-Oliviera J (2006) Antifungal activity of the essential oil of Thymus puleigoides on Candida, Aspergillus and dermatophyte species. J Med Microbiol 55:1367–1373

    Article  CAS  PubMed  Google Scholar 

  12. 12.

    Tavares AC, Gonçalves MJ, Cavaleiro C, Cruz MT, Lopes MC, Canhoto J, Salgueiro LR (2008) Essential oil of Daucus carota subsp. halophilus: composition, antifungal activity and cytotoxicity. J Ethnopharmacol 119:129–134

    Article  CAS  PubMed  Google Scholar 

  13. 13.

    Burt S (2004) Essential oils: their antibacterial properties and potential applications in foods—a review. Int J Food Microbiol 94:223–253

    Article  CAS  PubMed  Google Scholar 

  14. 14.

    Carson CF, Hammer KA, Riley TV (2006) Melaleuca alternifolia (tea tree) oil: a review of antimicrobial and other medicinal properties. Clin Microbiol Rev 19:50–62

    Article  CAS  PubMed  Google Scholar 

  15. 15.

    Liu K, Rossi PG, Ferrari B, Berti L, Casanova J, Tomi F (2007) Composition, irregular terpenoids, chemical variability and antibacterial activity of the essential oil from Santolina corsica Jordan et Fourr. Phytochemistry 68:1698–1705

    Article  CAS  PubMed  Google Scholar 

  16. 16.

    Rossi PG, Bao L, Luciani A, Panighi J, Desjobert JM, Costa J, Casanova J, Bolla JM, Berti L (2007) (E)-Methylisoeugenol and elemicin: antibacterial components of Daucus carota L. essential oil against Campylobacter jejuni. J Agric Food Chem 55:7332–7336

    Article  CAS  PubMed  Google Scholar 

  17. 17.

    Rossi PG, Berti L, Panighi J, Luciani A, Maury J, Muselli A, De Rocca SD, Gonny M, Bolla JM (2007) Antibacterial action of essential oils from Corsica. J Essent Oil Res 19:176–182

    CAS  Google Scholar 

  18. 18.

    Bianchini A, Tomi P, Costa J, Bernardini AF (2001) Composition of Helichrysum italicum (Roth) G. Don fil. subsp. italicum essential oils from Corsica (France). Flavour Fragr J 16:30–34

    Article  CAS  Google Scholar 

  19. 19.

    Blanc MC, Muselli A, Bradesi P, Casanova J (2004) Chemical composition and variability of the essential oil of Inula graveolens from Corsica. Flavour Fragr J 19:314–319

    Article  CAS  Google Scholar 

  20. 20.

    Carson CF, Hammer KA, Riley TV (1995) Broth micro-dilution method for determining the susceptibility of Escherichia coli and Staphylococcus aureus to the essential oil of Melaleuca alternifolia (tea tree oil). Microbios 82:181–185

    CAS  PubMed  Google Scholar 

  21. 21.

    Cha JD, Jung EK, Kil BS, Lee KY (2007) Chemical composition and antibacterial activity of essential oil from Artemisia feddei. J Microbiol Biotechnol 17:2061–2065

    CAS  PubMed  Google Scholar 

  22. 22.

    Klepser M, Ernst EJ, Russell EL, Ernst ME, Pfaller MA (1998) Influence of test conditions on antifungal time-kill curves results: proposal for standardized methods. Antimicrob Agents Chemother 42:1207–1212

    CAS  PubMed  Google Scholar 

  23. 23.

    Viljoen A, Van Vuuren S, Ernst E, Klepser M, Demirci B, Baser H, Van Wyk BE (2003) Osmitopsis asteriscoides (Asteraceae)—the antimicrobial activity and essential oil composition of a Cape-Dutch remedy. J Ethnopharmacol 88:137–143

    Article  CAS  PubMed  Google Scholar 

  24. 24.

    Carson CF, Mee BJ, Riley TV (2002) Mechanism of action of Melaleuca alternifolia (tea tree) oil on Staphylococcus aureus determined par time-kill, lysis, leakage and salt tolerance assays and electron microscopy. Antimicrob Agents Chemother 46:1914–1920

    Article  CAS  PubMed  Google Scholar 

  25. 25.

    National Commitee for Clinical Laboratory Standards (1999) Methods for determining bactericidal activity of antimicrobial agents. Approved guideline M26-A. NCCLS 19(18)

  26. 26.

    Hammer KA, Carson CF, Riley TV (1996) Susceptibility of transient and skin flora to the essential oil of Melaleuca alternifolia (tea tree oil). Am J Infect Control 24:186–189

    Article  CAS  PubMed  Google Scholar 

  27. 27.

    Garnier G, Bezanger-Beauquesne L, Debraux G (1961) Ressources médicinales de la flore Française. Vigot Frères Editeurs, Paris, vol. 2, pp 1358.

  28. 28.

    Bolhmann F, Mahanta PK, Jakupovic J, Rastogi RC, Natu AA (1978) Naturally occurring terpene derivatives. 142. New sesquiterpene lactones from Inula species. Phytochemistry 17:1165–1168

    Article  Google Scholar 

  29. 29.

    Dorman HJD, Deans SG (2000) Antimicrobial agents from plants: antibacterial activity of plant volatile oils. J Appl Microbiol 88:308–316

    Article  CAS  PubMed  Google Scholar 

  30. 30.

    Tabanca N, Kirimer N, Demirci F, Baser KH (2001) Composition and antimicrobial activity of the essential oil of Micromeria cristata subsp. phrygia and the enantiomeric distribution of borneol. J Agric Food Chem 49:4300–4003

    Article  CAS  PubMed  Google Scholar 

  31. 31.

    Debat J, Lemoine J, Lier-Gabillot F (1981) Inula extract, its method of preparation and its use as pharmaceutical. US Patent 4254112.

  32. 32.

    Caldes G, Prescott B, King JR (1975) Potential antileukemic substance present globularia alypum. Planta Med 27:72–76

    Article  CAS  PubMed  Google Scholar 

  33. 33.

    Arrigoni PV (1979) Le genre Santolina L. en Italie. Webbia 34:257–264

    Google Scholar 

  34. 34.

    Marino M, Bersani C, Comi G (2001) Impedance measurements to study the antimicrobial activity of essential oils from Lamiaceae and Compositae. Int J Food Microbiol 67:187–195

    Article  CAS  PubMed  Google Scholar 

  35. 35.

    Denyer SP, Hugo WB (1991) Biocide-induced damage to the bacterial cytoplasmic membrane. In: Denyer SP, Hugo WB (eds) Mechanisms of action of chemical biocides: their study and exploitation. Blackwell Scientific Publications, Oxford, United Kingdom, pp 171–187

    Google Scholar 

  36. 36.

    Hamouda T, Baker JR (2000) Antimicrobial mechanism of action of surfactant lipid preparations in enteric Gram-negative bacilli. J Applied Microbiol 89:397–403

    Article  CAS  Google Scholar 

  37. 37.

    Song MJ, Kim NM (2003) Antimicrobial action of p-hydroxyphenyl acrylate. Int Biodeterior Biodegradation 52:107–113

    Article  CAS  Google Scholar 

  38. 38.

    Razzaghi-Abyaneh M, Shams-Ghahfarokhi MK, Kawachi M, Eslamifar A, Schmidt OJ, Schmidt A, Allameh A, Yoshinari T (2006) Ultrastructural evidences of growth inhibitory effects of a novelbiocide, Akacids®plus, on an aflatoxigenic Aspergillus parasiticus. Toxicon 48:1075–1082

    Article  CAS  PubMed  Google Scholar 

  39. 39.

    Horne DS, Holm M, Oberg C, Chao S, Young DG (2001) Antimicrobial effects of essential oils on Streptococcus pneumoniae. J Essent Oil Res 13:387–392

    CAS  Google Scholar 

  40. 40.

    Windholz M, Budavari S, Blumetti RF, Otterbein ES (1983) The Merck index, 10th edn. Merck & Co, Inc., Rahway, NJ

    Google Scholar 

  41. 41.

    Reichling J, Weseler A, Landvatter U, Saller R (2002) Bioactive essential oils used in phytomedicine as antiinfective agents: Australian tea tree oil and manuka oil. Acta Phytotherapeutica 1:26–32

    Google Scholar 

  42. 42.

    Maisner-Patin S, Richard J (1996) Cell wall changes in nisin-resistant variants of Listeria monocytogenes grown in the presence of high nisin concentrations. FEMS Microbiol Lett 140:29–35

    Article  Google Scholar 

  43. 43.

    Calderόn-Miranda ML, Barbosa-Cánovas GV, Swanson BG (1999) Transmission electron microscopy of Listeria monocytogenes treated by pulsed electric fields and nisin in skimmed milk. Int J Food Microbiol 51:31–38

    Article  Google Scholar 

  44. 44.

    Sikkema J, De Bont JAM, Poolman B (1994) Interactions of cyclic hydrocarbons with biological membranes. J Biol Chem 269:8022–8028

    CAS  PubMed  Google Scholar 

  45. 45.

    Sikkema J, De Bont JAM, Poolman B (1995) Mechanism of membrane toxicity of hydrocarbons. Microbiol Rev 59:201–222

    CAS  PubMed  Google Scholar 

  46. 46.

    Cox SD, Mann CM, Markham JL, Bell HC, Gustafson JE, Warmington JR, Wyllie SG (2000) The mode of antimicrobial action of the essential oil of Melaleuca alternifolia (tea tree oil). J Appl Microbiol 88:170–175

    Article  CAS  PubMed  Google Scholar 

  47. 47.

    Ultee A, Bennink MJH, Moezelaar R (2002) The phenolic hydroxyl group of carvacrol is essential for action against the food-borne pathogene Bacillus cereus. Appl Env Microbiol 68:1561–1568

    Article  CAS  Google Scholar 

  48. 48.

    Kalemba D, Kunicka A (2003) Antibacterial and antifungal properties of essential oils. Curr Med Chem 10:813–829

    Article  CAS  PubMed  Google Scholar 

  49. 49.

    Cristani M, D'Arrigo M, Mandalari G, Castelli F, Sarpietro MG, Micieli D, Venuti V, Bisignano G, Saija A, Trombetta D (2007) Interaction of four monoterpenes contained in essential oils with model membranes: implications for their antibacterial activity. J Agric Food Chem 55:6300–6308

    Article  CAS  PubMed  Google Scholar 

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Acknowledgement

We would like to thank Pr. B. Marchand from the University of Corsica for the supply of the transmission electron microscopy equipment, and Mrs. A. Cornillac from the CMEABG of C. Bernard University (Lyon) for her expertise on the TEM experiments.

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Correspondence to A. Luciani.

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Guinoiseau, E., Luciani, A., Rossi, P.G. et al. Cellular effects induced by Inula graveolens and Santolina corsica essential oils on Staphylococcus aureus . Eur J Clin Microbiol Infect Dis 29, 873–879 (2010). https://doi.org/10.1007/s10096-010-0943-x

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Keywords

  • Minimum Inhibitory Concentration
  • Carvacrol
  • Minimum Bactericidal Concentration
  • Borneol
  • Myrcene