Individual constituents from essential oils inhibit biofilm mass production by multi-drug resistant staphylococcus aureus

Molecules

Volumn 20, Issue 6, 2015, Pages 11357-11372

  Espina, Laura ^a,b   Pagán, Rafael ^a,b   López, Daniel ^c   García Gonzalo, Diego ^a,b  

^a UNIVERSIDAD DE ZARAGOZA   (Spain)

^b UNIVERSITY OF ZARAGOZA   (Spain)

^c UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

(+) limonene; Biofilms; Carvacrol; citral; Essential oils; Staphylococcus aureus

Indexed keywords

ANTIINFECTIVE AGENT; CARVACROL; CITRAL; CYCLOHEXENE DERIVATIVE; ESSENTIAL OIL; LIMONENE; TERPENE;

BIOFILM; CHEMISTRY; DRUG EFFECTS; HUMAN; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIOLOGY; MULTIDRUG RESISTANCE; STAPHYLOCOCCAL INFECTIONS;

ANTI-INFECTIVE AGENTS; BIOFILMS; CYCLOHEXENES; DRUG RESISTANCE, MULTIPLE; HUMANS; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MONOTERPENES; OILS, VOLATILE; STAPHYLOCOCCAL INFECTIONS; TERPENES;

EID: 84938265859     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules200611357     Document Type: Article

References (59)

1. Costerton, J.; Stewart, P.S.; Greenberg, E. Bacterial biofilms: A common cause of persistent infections. Science 1999, 284, 1318-1322.
2. Srey, S.; Jahid, I.K.; Ha, S.D. Biofilm formation in food industries: A food safety concern. Food Control 2013, 31, 572-585.
3. Smith, K.; Perez, A.; Ramage, G.; Lappin, D.; Gemmell, C.G.; Lang, S. Biofilm formation by Scottish clinical isolates of Staphylococcus aureus. J. Med. Microbiol. 2008, 57, 1018-1023.
4. Otto, M. Basis of virulence in community-associated methicillin-resistant Staphylococcus aureus. Annu. Rev. Microbiol. 2010, 64, 143-162.
5. Lopez, D.; Vlamakis, H.; Kolter, R. Biofilms. Cold Spring Harb. Perspect. Biol. 2010, 2, a000398.
6. Van Houdt, R.; Michiels, C.W. Biofilm formation and the food industry, a focus on the bacterial outer surface. J. Appl. Microbiol. 2010, 109, 1117-1131.
7. Kluytmans, J.A.J.W. Methicillin-resistant Staphylococcus aureus in food products: Cause for concern or case for complacency? Clin. Microbiol. Infect. 2010, 16, 11-15.
8. Fratamico, P.M.; Annous, B.A.; Guenther, N. Biofilm formation by Gram-positive bacteria. In Biofilms in the Food and Beverage Industries; Woodhead Publishing Limited: Cambridge, UK, 2009.
9. Karatan, E.; Watnick, P. Signals, regulatory networks, and materials that build and break bacterial biofilms. Microbiol. Mol. Biol. Rev. 2009, 73, 310-347.
10. Köck, R.; Becker, K.; Cookson, B.; van Gemert-Pijnen, J.; Harbarth, S.; Kluytmans, J.; Mielke, M.; Peters, G.; Skov, R.; Struelens, M. Methicillin-resistant Staphylococcus aureus (MRSA): Burden of disease and control challenges in europe. Eurosurveillance 2010, 15, 19688.
11. Kumar, C.G.; Anand, S. Significance of microbial biofilms in food industry: A review. Int. J. Food Microbiol. 1998, 42, 9-27.
12. Caballero Gómez, N.; Abriouel, H.; Grande, M.J.; Pérez Pulido, R.; Gálvez, A. Combined treatments of enterocin AS-48 with biocides to improve the inactivation of methicillin-sensitive and methicillin-resistant Staphylococcus aureus planktonic and sessile cells. Int. J. Food Microbiol. 2013, 163, 96-100.
13. Burt, S. Essential oils: Their antibacterial properties and potential applications in foods-A review. Int. J. Food Microbiol. 2004, 94, 223-253.
14. Simoes, M.; Simoes, L.C.; Vieira, M.J. A review of current and emergent biofilm control strategies. LWT Food Sci. Technol. 2010, 43, 573-583.
15. Lang, G.; Buchbauer, G. A review on recent research results (2008-2010) on essential oils as antimicrobials and antifungals. A review. Flavour Fragr. J. 2012, 27, 13-39.
16. Adukwu, E.C.; Allen, S.C.; Phillips, C.A. The anti-biofilm activity of lemongrass (Cymbopogon flexuosus) and grapefruit (Citrus paradisi) essential oils against five strains of Staphylococcus aureus. J. Appl. Microbiol. 2012, 113, 1217-1227.
17. Kerekes, E.B.; Deák, É.; Takó, M.; Tserennadmid, R.; Petkovits, T.; Vágvölgyi, C.; Krisch, J. Anti-biofilm forming and anti-uorum sensing activity of selected essential oils and their main components on food-related micro-rganisms. J. Appl. Microbiol. 2013, 115, 933-942.
18. O'Toole, G.; Kaplan, H.B.; Kolter, R. Biofilm formation as microbial development. Annu. Rev. Microbiol. 2000, 54, 49-79.
19. Fisher, K.; Phillips, C. Potential antimicrobial uses of essential oils in food: Is citrus the answer? Trends Food Sci. Technol. 2008, 19, 156-164.
20. Espina, L.; Somolinos, M.; Lorán, S.; Conchello, P.; García, D.; Pagán, R. Chemical composition of commercial citrus fruit essential oils and evaluation of their antimicrobial activity acting alone or in combined processes. Food Control 2011, 22, 896-902.
21. Ait-Ouazzou, A.; Espina, L.; Gelaw, T.; Lamo-Castellví, S.; Pagán, R.; García-Gonzalo, D. New insights in mechanisms of bacterial inactivation by carvacrol. J. Appl. Microbiol. 2013, 114, 173-185.
22. Laird, K.; Armitage, D.; Phillips, C. Reduction of surface contamination and biofilms of Enterococcus sp. and Staphylococcus aureus using a citrus-based vapour. J. Hosp. Infect. 2012, 80, 61-66.
23. Landini, P.; Antoniani, D.; Burgess, J.G.; Nijland, R. Molecular mechanisms of compounds affecting bacterial biofilm formation and dispersal. Appl. Microbiol. Biotechnol. 2010, 86, 813-823.
24. Dong, L.; Tong, Z.; Linghu, D.; Lin, Y.; Tao, R.; Liu, J.; Tian, Y.; Ni, L. Effects of sub-minimum inhibitory concentrations of antimicrobial agents on Streptococcus mutans biofilm formation. Int. J. Antimicrob. Agents 2012, 39, 390-395.
25. Hoffman, L.R.; D'Argenio, D.A.; MacCoss, M.J.; Zhang, Z.; Jones, R.A.; Miller, S.I. Aminoglycoside antibiotics induce bacterial biofilm formation. Nature 2005, 436, 1171-1175.
26. Aiemsaard, J.; Aiumlamai, S.; Aromdee, C.; Taweechaisupapong, S.; Khunkitti, W. The effect of lemongrass oil and its major components on clinical isolate mastitis pathogens and their mechanisms of action on Staphylococcus aureus dmst 4745. Res. Vet. Sci. 2011, 91, e31-e37.
27. Nostro, A.; Roccaro, A.S.; Bisignano, G.; Marino, A.; Cannatelli, M.A.; Pizzimenti, F.C.; Cioni, P.L.; Procopio, F.; Blanco, A.R. Effects of oregano, carvacrol and thymol on Staphylococcus aureus and Staphylococcus epidermidis biofilms. J. Med. Microbiol. 2007, 56, 519-523.
28. Soni, K.A.; Oladunjoye, A.; Nannapaneni, R.; Schilling, M.; Silva, J.L.; Mikel, B.; Bailey, R. Inhibition and inactivation of Salmonella Typhimurium biofilms from polystyrene and stainless steel surfaces by essential oils and phenolic constituent carvacrol. J. Food Prot. 2013, 76, 205-212.
29. Rode, T.M.; Langsrud, S.; Holck, A.; Møretrø, T. Different patterns of biofilm formation in Staphylococcus aureus under food-related stress conditions. Int. J. Food Microbiol. 2007, 116, 372-383.
30. Vázquez-Sánchez, D.; Habimana, O.; Holck, A. Impact of food-related environmental factors on the adherence and biofilm formation of natural Staphylococcus aureus isolates. Curr. Microbiol. 2013, 66, 110-121.
31. Lebert, I.; Leroy, S.; Talon, R. Effect of industrial and natural biocides on spoilage, pathogenic and technological strains grown in biofilm. Food Microbiol. 2007, 24, 281-287.
32. Al-Shuneigat, J.; Cox, S.D.; Markham, J.L. Effects of a topical essential oil-containing formulation on biofilm-forming coagulase-negative staphylococci. Lett. Appl. Microbiol. 2005, 41, 52-55.
33. Nostro, A.; Scaffaro, R.; D'Arrigo, M.; Botta, L.; Filocamo, A.; Marino, A.; Bisignano, G. Study on carvacrol and cinnamaldehyde polymeric films: Mechanical properties, release kinetics and antibacterial and antibiofilm activities. Appl. Microbiol. Biotechnol. 2012, 96, 1029-1038.
34. Schillaci, D.; Napoli, E.M.; Cusimano, M.G.; Vitale, M.; Ruberto, A. Origanum vulgare subsp. hirtum essential oil prevented biofilm formation and showed antibacterial activity against planktonic and sessile bacterial cells. J. Food Prot. 2013, 76, 1747-1752.
35. Lee, K.; Lee, J.-H.; Kim, S.-I.; Cho, M.; Lee, J. Anti-biofilm, anti-hemolysis, and anti-virulence activities of black pepper, cananga, myrrh oils, and nerolidol against Staphylococcus aureus. Appl. Microbiol. Biotechnol. 2014, 98, 9447-9457.
36. Chorianopoulos, N.G.; Giaouris, E.D.; Skandamis, P.N.; Haroutounian, S.A.; Nychas, G.J.E. Disinfectant test against monoculture and mixed-culture biofilms composed of technological, spoilage and pathogenic bacteria: Bactericidal effect of essential oil and hydrosol of Satureja thymbra and comparison with standard acid-base sanitizers. J. Appl. Microbiol. 2008, 104, 1586-1596.
37. Burt, S.A.; Ojo-Fakunle, V.T.A.; Woertman, J.; Veldhuizen, E.J.A. The natural antimicrobial carvacrol inhibits quorum sensing in Chromobacterium violaceum and reduces bacterial biofilm formation at sub-lethal concentrations. PLoS ONE 2014, 9, e93414.
38. Giaouris, E.; Chorianopoulos, N.; Nychas, G.J. Acquired acid adaptation of Listeria monocytogenes during its planktonic growth enhances subsequent survival of its sessile population to disinfection with natural organic compounds. Food Res. Int. 2014, 64, 896-900.
39. Kavanaugh, N.L.; Ribbeck, K. Selected antimicrobial essential oils eradicate Pseudomonas spp. and Staphylococcus aureus biofilms. Appl. Environ. Microbiol. 2012, 78, 4057-4061.
40. Niu, C.; Gilbert, E. Colorimetric method for identifying plant essential oil components that affect biofilm formation and structure. Appl. Environ. Microbiol. 2004, 70, 6951-6956.
41. Sandasi, M.; Leonard, C.; Viljoen, A. The effect of five common essential oil components on Listeria monocytogenes biofilms. Food Control 2008, 19, 1070-1075.
42. Sandasi, M.; Leonard, C.; Van Vuuren, S.; Viljoen, A. Peppermint (Mentha piperita) inhibits microbial biofilms in vitro. S. Afr. J. Bot. 2011, 77, 80-85.
43. Harvey, J.; Keenan, K.; Gilmour, A. Assessing biofilm formation by Listeria monocytogenes strains. Food Microbiol. 2007, 24, 380-392.
44. Jackson, D.W.; Suzuki, K.; Oakford, L.; Simecka, J.W.; Hart, M.E.; Romeo, T. Biofilm formation and dispersal under the influence of the global regulator Csra of Escherichia coli. J. Bacteriol. 2002, 184, 290-301.
45. Kreiswirth, B.; Kornblum, J.; Arbeit, R.D.; Eisner, W.; Maslow, J.N.; McGeer, A.; Low, D.E.; Novick, R.P. Evidence for a clonal origin of methicillin resistance in Staphylococcus aureus. Science 1993, 259, 227-230.
46. Klevens, R.M.; Morrison, M.A.; Nadle, J.; Petit, S.; Gershman, K.; Ray, S.; Harrison, L.H.; Lynfield, R.; Dumyati, G.; Townes, J.M.; et al. Invasive methicillin-resistant Staphylococcus aureus infections in the United States. J. Am. Med. Assoc. 2007, 298, 1763-1771.
47. Diep, B.A.; Chambers, H.F.; Graber, C.J.; Szumowski, J.D.; Miller, L.G.; Han, L.L.; Chen, J.H.; Lin, F.; Lin, J.; Phan, T.H.; et al. Emergence of multidrug-resistant, community-associated, methicillin-resistant Staphylococcus aureus clone USA300 in men who have sex with men. Ann. Intern. Med. 2008, 148, 249-257.
48. Sacchetti, G.; Maietti, S.; Muzzoli, M.; Scaglianti, M.; Manfredini, S.; Radice, M.; Bruni, R. Comparative evaluation of 11 essential oils of different origin as functional antioxidants, antiradicals and antimicrobials in foods. Food Chem. 2005, 91, 621-632.
49. Kuorwel, K.K.; Cran, M.J.; Sonneveld, K.; Miltz, J.; Bigger, S.W. Essential oils and their principal constituents as antimicrobial agents for synthetic packaging films. J. Food Sci. 2011, 76, R164-R177.
50. Koch, G.; Yepes, A.; Forstner, K.U.; Wermser, C.; Stengel, S.T.; Modamio, J.; Ohlsen, K.; Foster, K.R.; Lopez, D. Evolution of resistance to a last-resort antibiotic in Staphylococcus aureus via bacterial competition. Cell 2014, 158, 1060-1071.
51. Ohno, T.; Kita, M.; Yamaoka, Y.; Imamura, S.; Yamamoto, T.; Mitsufuji, S.; Kodama, T.; Kashima, K.; Imanishi, J. Antimicrobial activity of essential oils against Helicobacter pylori. Helicobacter 2003, 8, 207-215.
52. Duthie, E.S.; Haughton, G. Purification of free staphylococcal coagulase. Biochem. J. 1958, 70, 125-134.
53. Gillaspy, A.F.; Hickmon, S.G.; Skinner, R.A.; Thomas, J.R.; Nelson, C.L.; Smeltzer, M.S. Role of the accessory gene regulator (agr) in pathogenesis of staphylococcal osteomyelitis. Infect. Immun. 1995, 63, 3373-3380.
54. Beenken, K.E.; Blevins, J.S.; Smeltzer, M.S. Mutation of sarA in Staphylococcus aureus limits biofilm formation. Infect. Immun. 2003, 71, 4206-4211.
55. Diep, B.A.; Gill, S.R.; Chang, R.F.; Phan, T.H.; Chen, J.H.; Davidson, M.G.; Lin, F.; Lin, J.; Carleton, H.A.; Mongodin, E.F. Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet 2006, 367, 731-739.
56. O'Toole, G.A.; Kolter, R. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 1998, 30, 295-304.
57. O'Toole, G.A. Microtiter dish biofilm formation assay. J. Vis. Exp. 2011, doi:10.3791/2437.
58. Kwasny, S.M.; Opperman, T.J. Static biofilm cultures of gram-positive pathogens grown in a microtiter format used for anti-biofilm drug discovery. Curr. Protoc. Pharmacol. 2010, 50, 13A.18.11-13A.18.23.
59. Pruessner, J.C.; Kirschbaum, C.; Meinlschmid, G.; Hellhammer, D.H. Two formulas for computation of the area under the curve represent measures of total hormone concentration versus time-dependent change. Psychoneuroendocrinology 2003, 28, 916-931.