Antibacterial and efflux pump inhibitors of thymol and carvacrol against food-borne pathogens

Microbial Pathogenesis

Volumn 99, Issue , 2016, Pages 95-100

  Miladi, Hanene ^a   Zmantar, Tarek ^a   Chaabouni, Yassine ^b   Fedhila, Kais ^a   Bakhrouf, Amina ^a   Mahdouani, Kacem ^a,b   Chaieb, Kamel ^c  

^a UNIVERSITY OF MONASTIR   (Tunisia)

^b Ibn Al Jazzar Hospital   (Tunisia)

^c TAIBAH UNIVERSITY   (Saudi Arabia)

Author keywords

Antimicrobial activity; Carvacrol; Efflux pump inhibitors; Multidrug resistant; Thymol

Indexed keywords

ANTIINFECTIVE AGENT; BENZALKONIUM CHLORIDE; CARVACROL; EFFLUX PUMP INHIBITOR; ETHIDIUM BROMIDE; TETRACYCLINE; THYMOL; UNCLASSIFIED DRUG; BENZALKONIUM; ETHIDIUM; PLANT MEDICINAL PRODUCT; TERPENE;

ANTIBACTERIAL ACTIVITY; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACILLUS CEREUS; BACTERIAL STRAIN; CELL TRANSPORT; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG POTENCY; DRUG POTENTIATION; ENTEROCOCCUS FAECALIS; ESCHERICHIA COLI; FOOD BORNE BACTERIUM; FOOD SPOILAGE; IC50; MINIMUM BACTERICIDAL CONCENTRATION; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PRIORITY JOURNAL; PROKARYOTES BY HABITAT; PSEUDOMONAS AERUGINOSA; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS; VIBRIO ALGINOLYTICUS; ACTIVE TRANSPORT; BACTERIUM; DRUG EFFECTS; FOOD POISONING; ISOLATION AND PURIFICATION; METABOLISM; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY;

ANTI-INFECTIVE AGENTS; BACTERIA; BENZALKONIUM COMPOUNDS; BIOLOGICAL TRANSPORT, ACTIVE; DRUG SYNERGISM; ETHIDIUM; FOODBORNE DISEASES; INHIBITORY CONCENTRATION 50; MICROBIAL SENSITIVITY TESTS; MONOTERPENES; PHYTOCHEMICALS; TETRACYCLINE; THYMOL;

EID: 84982239127     PISSN: 08824010     EISSN: 10961208     Source Type: Journal    
DOI: 10.1016/j.micpath.2016.08.008     Document Type: Article

References (36)

1. [1] Miladi, H., Ben Slama, R., Mili, D., Zouari, S., Bakhrouf, A., Ammar, E., Essential oil of Thymus vulgaris L. and Rosmarinus officinalis L.: gas chromatography-mass spectrometry analysis, cytotoxicity and antioxidant properties and antibacterial activities against foodborne pathogens. Nat. Sci. 5 (2013), 729–739.
2. [2] Miladi, H., Mili, D., Ben Slama, R., Zouari, S., Ammar, E., Bakhrouf, A., Antibiofilm formation and anti-adhesive property of three mediterranean essential oils against a foodborne pathogen Salmonella strain. Microb. Pathog. 93 (2016), 22–31.
3. [3] Solórzano-Santos, F., Miranda-Novales, M.G., Essential oils from aromatic herbs as antimicrobial agents. Curr. Opin. Biotechnol. 23 (2012), 136–141.
4. [4] Schindler, B.D., Jacinto, P., Kaatz, G.W., Inhibition of drug efflux pumps in Staphylococcus aureus: current status of potentiating existing antibiotics. Future Microbiol. 8 (2013), 491–507.
5. [5] Gould, I.M., David, M.Z., Esposito, S., Garau, J., Lina, G., Mazzei, T., Peters, G., New insights into meticillin-resistant Staphylococcus aureus (MRSA) pathogenesis, treatment and resistance. Int. J. Antimicrob. Agents 39 (2012), 96–104.
6. [6] Kumar, S., Mukherjee, M.M., Varela, M.F., Modulation of bacterial multidrug resistance efflux pumps of the major facilitator superfamily. Int. J. Bacteriol. 2013 (2013), 1–15.
7. [7] Stavri, M., Piddock, L.J., Gibbons, S., Bacterial efflux pump inhibitors from natural sources. J. Antimicrob. Chemother. 59 (2007), 1247–1260.
8. [8] Kouidhi, B., Zmantar, T., Jrah, H., Souiden, Y., Chaieb, K., Mahdouani, K., Bakhrouf, A., Antibacterial and resistance-modifying activities of thymoquinone against oral pathogens. Ann. Clin. Microbiol. Antimicrob. 10 (2011), 29–35.
9. [9] Oluwatuyi, M., Kaatz, G.W., Gibbons, S., Antibacterial and resistance modifying activity of Rosmarinus officinalis. Phytochemistry 65 (2004), 3249–3254.
10. [10] Lee, Y.-S., Han, S.-H., Lee, S.-H., Kim, Y.-G., Park, C.-B., Kang, O.-H., Keum, J.-H., Kim, S.-B., Mun, S.-H., Shin, D.-W., Synergistic effect of tetrandrine and ethidium bromide against methicillin-resistant Staphylococcus aureus (MRSA). J. Toxicol. Sci. 36 (2011), 645–651.
11. [11] Roy, S.K., Kumari, N., Pahwa, S., Agrahari, U.C., Bhutani, K.K., Jachak, S.M., Nandanwar, H., NorA efflux pump inhibitory activity of coumarins from Mesua ferrea. Fitoterapia 90 (2013), 140–150.
12. [12] Kesherwani, M., Gromiha, M.M., Fukui, K., Velmurugan, D., Identification of novel natural inhibitor for NorM–A Multidrug and Toxic compound extrusion Transporter-An insilico molecular modeling and simulation studies. J. Biomol. Struct. Dyn. 20 (2016), 1–47.
13. [13] Gholijani, N., Gharagozloo, M., Kalantar, F., Ramezani, A., Amirghofran, Z., Modulation of cytokine production and transcription factors activities in human jurkat t cells by thymol and carvacrol. Adv. Pharm. Bull. 5 (2015), 653–660.
14. [14] Lambert, R., Skandamis, P.N., Coote, P.J., Nychas, G.J., Study of the minimum inhibitory concentration and mode of action of oregano essential oil, thymol and carvacrol. J. Appl. Microbiol. 91 (2001), 453–462.
15. [15] Johny, A.K., Hoagland, T., Venkitanarayanan, K., Effect of subinhibitory concentrations of plant-derived molecules in increasing the sensitivity of multidrug-resistant Salmonella enterica serovar Typhimurium DT104 to antibiotics. Foodborne Pathog. Dis. 7 (2010), 1165–1170.
16. [16] Trombetta, D., Castelli, F., Sarpietro, M.G., Venuti, V., Cristani, M., Daniele, C., Saija, A., Mazzanti, G., Bisignano, G., Mechanisms of antibacterial action of three monoterpenes. Antimicrob. Agents Chemother. 49 (2005), 2474–2478.
17. [17] Ultee, A., Bennik, M., Moezelaar, R., The phenolic hydroxyl group of carvacrol is essential for action against the food-borne pathogen Bacillus cereus. Appl. Environ. Microbiol. 68 (2002), 1561–1568.
18. [18] Ultee, A., Kets, E.P., Alberda, M., Hoekstra, F.A., Smid, E.J., Adaptation of the food-borne pathogen Bacillus cereus to carvacrol. Arch. Microbiol. 174 (2000), 233–238.
19. [19] Ultee, A., Slump, R., Steging, G., Smid, E., Antimicrobial activity of carvacrol toward Bacillus cereus on rice. J. Food Prot. 63 (2000), 620–624.
20. [20] Suntres, Z.E., Coccimiglio, J., Alipour, M., The bioactivity and toxicological actions of carvacrol. Crit. Rev. Food. Sci. Nutr. 55 (2015), 304–318.
21. [21] Cirino, I.C.S., Menezes-Silva, S.M.P., Silva, H.T.D., de Souza, E.L., Siqueira-Júnior, J.P., The essential oil from Origanum vulgare L. and its individual constituents carvacrol and thymol enhance the effect of tetracycline against Staphylococcus aureus. Chemotherapy 60 (2014), 290–293.
22. [22] Lorenzi, V., Muselli, A., Bernardini, A.F., Berti, L., Pagès, J.-M., Amaral, L., Bolla, J.-M., Geraniol restores antibiotic activities against multidrug-resistant isolates from gram-negative species. Antimicrob. Agents Chemother. 53 (2009), 2209–2211.
23. [23] Medeiros Barreto, H., Cerqueira Fontinele, F., Pereira de Oliveira, A., Arcanjo, D.D.R., Cavalcanti dos Santos, B.H., de Abreu, A.P.L., Douglas Melo Coutinho, H., Alves Carvalho da Silva, R., Oliveira de Sousa, T., Freire de Medeiros, M.D.G., Phytochemical prospection and modulation of antibiotic activity in vitro by Lippia origanoides HBK in methicillin resistant Staphylococcus aureus. Biomed. Res. Int. 2014 (2014), 1–7.
24. [24] CLSI, Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically. Approved Standard – Seventh Edition CLSI Document M7-A7. 2006.
25. [25] Magina, M.D., Dalmarco, E.M., Wisniewski, A.J.R., Simionatto, E.L., Dalmarco, J.B., Pizzolatti, M.G., Brighente, I.M., Chemical composition and antibacterial activity of essential oils of Eugenia species. J. Nat. Med. 63 (2009), 345–350.
26. [26] Al-hebshi, N., Al-haroni, M., Skaug, N., In vitro antimicrobial and resistance-modifying activities of aqueous crude khat extracts against oral microorganisms. Arch. Oral. Biol. 51 (2006), 183–188.
27. [27] Smith, H.E., Blair, J.M., Redundancy in the periplasmic adaptor proteins AcrA and AcrE provides resilience and an ability to export substrates of multidrug efflux. J. Antimicrob. Chemother. 69 (2013), 982–987.
28. [28] Rivas, L., McDonnell, M.J., Burgess, C.M., O'Brien, M., Navarro-Villa, A., Fanning, S., Duffy, G., Inhibition of verocytotoxigenic Escherichia coli in model broth and rumen systems by carvacrol and thymol. Int. J. Food Microbiol. 139 (2010), 70–78.
29. [29] Olasupo, N., Fitzgerald, D., Gasson, M., Narbad, A., Activity of natural antimicrobial compounds against Escherichia coli and Salmonella enterica serovar Typhimurium. Lett. Appl. Microbiol. 37 (2003), 448–451.
30. [30] Rattanachaikunsopon, P., Phumkhachorn, P., Assessment of factors influencing antimicrobial activity of carvacrol and cymene against Vibrio cholerae in food. J. Biosci. Bioeng. 110 (2010), 614–619.
31. [31] Jorgensen, J.H., Clinical, Institute LS. Methods for Antimicrobial Dilution and Disk Susceptibility Testing of Infrequently Isolated or Fastidious Bacteria: Approved Guideline. 2010, National Committee for Clinical Laboratory Standards.
32. [32] Soares de Oliveira, C., dos Santos Falcão-Silva, V., Siqueira-Júnior, J.P., Harding, D.P., Lira, B.F., Lorenzo, J.G.F., Barbosa-Filho, J.M., Filgueiras de Athayde-Filho, P., Drug resistance modulation in Staphylococcus aureus, a new biological activity for mesoionic hydrochloride compounds. Molecules 16 (2011), 2023–2031.
33. [33] Obaidat, R.M., Bader, A., Al-Rajab, W., Abu Sheikha, G., Obaidat, A.A., Preparation of mucoadhesive oral patches containing tetracycline hydrochloride and carvacrol for treatment of local mouth bacterial infections and candidiasis. Sci. Pharm. 79 (2011), 197–212.
34. [34] Giraud, E., Cloeckaert, A., Kerboeuf, D., Chaslus-Dancla, E., Evidence for active efflux as the primary mechanism of resistance to ciprofloxacin in Salmonella enterica serovar Typhimurium. Antimicrob. agents Chemother. 44 (2000), 1223–1228.
35. [35] Piddock, L.J., White, D.G., Gensberg, K., Pumbwe, L., Griggs, D.J., Evidence for an efflux pump mediating multiple antibiotic resistance in Salmonella enterica serovar Typhimurium. Antimicrob. Agents Chemother. 44 (2000), 3118–3121.
36. [36] Kaatz, G.W., Moudgal, V.V., Seo, S.M., Kristiansen, J.E., Phenothiazines and thioxanthenes inhibit multidrug efflux pump activity in Staphylococcus aureus. Antimicrob. Agents. Chemother. 47 (2003), 719–726.