Potential of Carvacrol and Thymol in Reducing Biofilm Formation on Technical Surfaces
Abstract
:1. Introduction
2. Results and Discussion
2.1. Screening Test
2.2. Total Biofilm Amount
2.3. Biofilm Hydrolytic Activity
2.4. Live and Dead Staining
3. Materials and Methods
3.1. Bacterial Strains Used in the Research
3.2. Tested Materials Types
3.3. Screening Test
3.4. Biofilm Formation on PVC, PE, PP and SS
3.5. Estimation of Total Biofilm Amount
3.6. Estimation of Biofilm Hydrolytic Activity
3.7. Live and Dead Staining
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Conflicts of Interest
Sample Availability
References
- Watnick, P.; Kolter, R. Biofilm, City of Microbes. J. Bacteriol. 2000, 182, 2675–2679. [Google Scholar] [CrossRef] [Green Version]
- Yin, W.; Wang, Y.; Liu, L.; He, J. Biofilms: The microbial “protective clothing” in extreme environments. Int. J. Mol. Sci. 2019, 20, 3423. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Marić, S.; Vraneš, J. Characteristics and significance of microbial biofilm formation. Period. Biol. 2007, 109, 115–121. [Google Scholar]
- Donlan, R.M.; Costerton, J.W. Biofilms: Survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 2002, 15, 167–193. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nandakumar, V.; Chittaranjan, S.; Kurian, V.M.; Doble, M. Characteristics of bacterial biofilm associated with implant material in clinical practice. Polym. J. 2012, 45, 137–152. [Google Scholar] [CrossRef] [Green Version]
- Jarząb, N.; Walczak, M.; Smoliński, D.; Sionkowska, A. The impact of medicinal brines on microbial biofilm formation on inhalation equipment surfaces. Biofouling 2018, 34, 963–975. [Google Scholar] [CrossRef]
- Khelissa, S.O.; Abdallah, M.; Jama, C.; Faille, C.; Chihib, N.E. Bacterial contamination and biofilm formation on abiotic surfaces and strategies to overcome their persistence. J. Mater. Environ. Sci. 2017, 10, 3326–3346. [Google Scholar]
- Feng, G.; Cheng, Y.; Wang, S.-Y.; Borca-Tasciuc, D.A.; Worobo, R.W.; Moraru, C.I. Bacterial attachment and biofilm formation on surfaces are reduced by small-diameter nanoscale pores: How small is small enough? Biofilms Microbiomes 2015, 1, 15022. [Google Scholar] [CrossRef]
- Petrova, O.E.; Sauer, K. Escaping the biofilm in more than one way: Desorption, detachment or dispersion. Curr. Opin. Microbiol. 2016, 30, 67–78. [Google Scholar] [CrossRef] [Green Version]
- Francolini, F.; Donelli, G. Prevention and control of biofilm-based medical-device-relate. FEMS Immunol. Med. Microbiol. 2010, 59, 227–238. [Google Scholar] [CrossRef] [Green Version]
- Marques, S.C.; Rezende, J.D.; Alves, L.A.; Silva, B.C.; Alves, E.; De Abreu, L.R.; Píccoli, R.H. Formation of biofilms by Staphylococcus aureus on stainless steel and glass surfaces and its resistance to some selected chemical sanitizers. Braz. J. Microbiol. 2007, 38, 538–543. [Google Scholar] [CrossRef] [Green Version]
- Mulcahy, L.R.; Isabella, V.M.; Lewis, K. Pseudomonas aeruginosa Biofilms in Disease. Microb. Ecol. 2014, 68, 1–12. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, Q.; Xie, S.; Lou, X.; Cheng, S.; Liu, X.; Zheng, W.; Zheng, Z.; Wang, H. Biofilm formation and prevalence of adhesion genes among Staphylococcus aureus isolates from different food sources. Microbiologyopen 2020, 9, e00946. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Diggle, S.P.; Whiteley, M. Microbe profile: Pseudomonas aeruginosa: Opportunistic pathogen and lab rat. Microbiology 2020, 166, 30–33. [Google Scholar] [CrossRef]
- Banerjee, M.; Moulick, S.; Bhattacharya, K.K.; Parai, D.; Chattopadhyay, S.; Mukherjee, S.K. Attenuation of Pseudomonas aeruginosa quorum sensing, virulence and biofilm formation by extracts of Andrographis paniculate. Microb. Pathog. 2017, 113, 85–93. [Google Scholar] [CrossRef]
- Al-Shabib, N.A.; Husain, F.M.; Ahmad, I.; Baig, M.H. Eugenol inhibits quorum sensing and biofilm of toxigenic MRSA strains isolated from food handlers employed in Saudi Arabia. Biotechnol. Biotechnol. Equip. 2017, 31, 387–396. [Google Scholar] [CrossRef] [Green Version]
- Wang, H.; Wang, H.; Liang, L.; Xu, X.; Zhou, G. Prevalence, genetic characterization and biofilm formation in vitro of Staph-ylococcus aureus isolated from raw chicken meat at retail level in Nanjing, China. Food Control 2018, 86, 11–18. [Google Scholar] [CrossRef]
- Tuttlebee, C.M.; O’Donnell, M.J.; Keane, C.T.; Russell, R.J.; Sullivan, D.J.; Falkiner, F.; Coleman, D.C. Effective control of dental chair unit waterline biofilm and marked reduction of bacterial contamination of output water photocatalytic ALD and sol-gel TiO(2) surfaces. J. Ind. Microbiol. Biotechnol. 2002, 52, 192–205. [Google Scholar]
- Carmen, J.C.; Nelson, J.L.; Beckstead, B.L.; Runyan, C.M.; Robison, R.A.; Schaalje, G.B.; Pitt, W.G. Ultrasonic-enhanced gen-tamicin transport through colony biofilms of Pseudomonas aeruginosa and Escherichia coli. J. Infect. Chemother. 2004, 10, 193–199. [Google Scholar] [CrossRef] [Green Version]
- Soumya, E.A.; Saad, I.K.; Hassan, L.; Ghizlane, Z.; Hind, M.; Adnane, R. Carvacrol and thymol components inhibiting Pseudomonas aeruginosa adherence and biofilm formation. Afr. J. Microbiol. Res. 2011, 5, 3229–3232. [Google Scholar]
- Inouye, S.; Takizawa, T.; Yamaguchi, H. Antibacterial activity of essential oils and their major constituents against respiratory tract pathogens by gaseous contact. J. Antimicrob. Chemother. 2001, 47, 565–573. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Miladi, H.; Zmantar, T.; Kouidhi, B.; Chaabouni, Y.; Mahdouani, K.; Bakhrouf, A.; Chaieb, K. Use of carvacrol, thymol, and eugenol for biofilm eradication and resistance modifying susceptibility of Salmonella enterica serovar Typhimurium strains to nalidixic acid. Microb. Pathog. 2017, 104, 56–63. [Google Scholar] [CrossRef]
- Meeran, M.F.N.; Javed, H.; Al Taee, H.; Azimullah, S.; Ojha, S.K. pharmacological properties and molecular mechanisms of thymol: Prospects for its therapeutic potential and pharmaceutical development. Front. Pharmacol. 2017, 8, 380. [Google Scholar] [CrossRef] [Green Version]
- Khan, S.T.; Khan, M.; Ahmad, J.; Wahab, R.; Abd-Elkader, O.H.; Musarrat, J.; Alkhathlan, H.Z.; Al-Kedhairy, A.A. Thymol and carvacrol induce autolysis, stress, growth inhibition and reduce the biofilm formation by Streptococcus mutans. AMB Express 2017, 7, 1–11. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kavanaugh, N.L.; Ribbeck, K. Selected antimicrobial essential oils eradicate Pseudomonas spp. and Staphylococcus aureus biofilms. Appl. Environ. Microbiol. 2012, 78, 4057–4061. [Google Scholar] [CrossRef] [Green Version]
- Pekmezovic, M.; Aleksic, I.; Barac, A.; Arsic-Arsenijevic, V.; Vasiljevic, B.; Nikodinovic-Runic, J.; Senerovic, L. Prevention of polymicrobial biofilms composed of Pseudomonas aeruginosa and pathogenic fungi by essential oils from selected Citrus species. Pathog. Dis. 2016, 74, 102. [Google Scholar] [CrossRef] [Green Version]
- Kumari, P.; Mishra, R.; Arora, N.; Chatrath, A.; Gangwar, R.; Roy, P.; Prasad, R. Antifungal and anti-biofilm activity of essential oil active components against Cryptococcus neoformans and Cryptococcus laurentii. Front. Microbiol. 2017, 8, 2161. [Google Scholar] [CrossRef] [PubMed]
- Raei, P.; Pourlak, T.; Memar, M.Y.; Alizadeh, N.; Aghamali, M.; Zeinalzadeh, E.; Asgharzadeh, M.; Kafil, H.S. Thymol and carvacrol strongly inhibit biofilm formation and growth of carbapenemase-producing Gram negative bacilli. Cell. Mol. Biol. 2017, 63, 108–112. [Google Scholar] [CrossRef] [PubMed]
- Roby, M.H.H.; Sarhan, M.A.; Selim, K.A.-H.; Khalel, K.I. Antioxidant and antimicrobial activities of essential oil and extracts of fennel (Foeniculum vulgare L.) and chamomile (Matricaria chamomilla L.). Ind. Crop. Prod. 2013, 44, 437–445. [Google Scholar] [CrossRef]
- Caleja, C.; Barros, L.; Antonio, A.L.; Ciric, A.; Soković, M.; Oliveira, M.B.P.; Santos-Buelga, C.; Ferreira, I.C. Foeniculum vulgare Mill. as natural conservation enhancer and health promoter by incorporation in cottage cheese. J. Funct. Foods 2015, 12, 428–438. [Google Scholar] [CrossRef]
- Koriem, K.M.M. Approach to pharmacological and clinical applications of Anisi aetheroleum. Asian Pac. J. Trop. Biomed. 2015, 5, 60–67. [Google Scholar] [CrossRef]
- Gülçin, I.; Oktay, M.; Kireçci, E.; Küfrevioǧlu, Ö.I. Screening of antioxidant and antimicrobial activities of anise (Pimpinella anisum L.) seed extracts. Food Chem. 2003, 83, 371–382. [Google Scholar] [CrossRef]
- Liu, H.; Lepoittevin, B.; Roddier, C.; Guerineau, V.; Bech, L.; Herry, J.-M.; Bellon-Fontaine, M.-N.; Roger, P. Facile synthesis and promising antibacterial properties of a new guaiacol-based polymer. Polymer 2011, 52, 1908–1916. [Google Scholar] [CrossRef]
- Dhara, L.; Tripathi, A. Antimicrobial activity of eugenol and cinnamaldehyde against extended spectrum beta lactamase producing enterobacteriaceae by in vitro and molecular docking analysis. Eur. J. Integr. Med. 2013, 5, 527–536. [Google Scholar] [CrossRef]
- Ben Arfa, A.; Combes, S.; Preziosi-Belloy, L.; Gontard, N.; Chalier, P. Antimicrobial activity of carvacrol related to its chemical structure. Lett. Appl. Microbiol. 2006, 43, 149–154. [Google Scholar] [CrossRef]
- Pinheiro, P.F.; Menini, L.A.P.; Bernardes, P.C.; Saraiva, S.H.; Carneiro, J.W.M.; Costa, A.V.; Alvarenga, E.S.; Lage, M.R.; Martins Gonçalves, P.; de Oliveira Bernardes, C. Semisynthetic phenol derivatives obtained from natural phenols: Antimi-crobial activity and molecular properties. J. Agric. Food Chem. 2017, 66, 323–330. [Google Scholar] [CrossRef]
- Griffin, S.; Grant, S.; Wyllie, J.; Markham, J. Determination of octanol–water partition coefficient for terpenoids using re-versed-phase high-performance liquid chromatography. J. Chromatogr. A 1999, 864, 221–228. [Google Scholar] [CrossRef]
- Engel, B.J.; Heckler, C.; Tondo, E.C.; Joner Daroit, D.; da Silva Malheiros, P. Antimicrobial activity of free and lipo-some-encapsulated thymol and carvacrol against Salmonella and Staphylococcus aureus adhered to stainless steel. Int. J. Food Microbiol. 2017, 252, 18–23. [Google Scholar] [CrossRef]
- Lambert, R.; Skandamis, P.; Coote, P.; Nychas, G.-J. A study of the minimum inhibitory concentration and mode of action of oregano essential oil, thymol and carvacrol. J. Appl. Microbiol. 2001, 91, 453–462. [Google Scholar] [CrossRef] [Green Version]
- Ahmad, A.; Khan, A.; Akhtar, F.; Yousuf, S.; Xess, I.; Khan, L.A.; Manzoor, N. Fungicidal activity of thymol and carvacrol by disrupting ergosterol biosynthesis and membrane integrity against Candida. Eur. J. Clin. Microbiol. Infect. Dis. 2010, 30, 41–50. [Google Scholar] [CrossRef]
- Upadhyay, A.; Upadhyaya, I.; Kollanoor-Johny, A.; Venkitanarayanan, K. Antibiofilm effect of plant derived antimicrobials on Listeria monocytogenes. Food Microbiol. 2013, 36, 79–89. [Google Scholar] [CrossRef] [PubMed]
- Wang, L.; Zhao, X.; Zhu, C.; Xia, X.; Qin, W.; Li, M.; Wang, T.; Chen, S.; Xu, Y.; Hang, B.; et al. Thymol kills bacteria, reduces biofilm formation, and protects mice against a fatal infection of Actinobacillus pleuropneumoniae strain L20. Vet. Microbiol. 2017, 203, 202–210. [Google Scholar] [CrossRef]
- de Oliveira, R.; Viegas, D.J.; Réquia Martins, A.P.; Talge Carvalho, C.A.; Pacheco Soares, C.; Afonso Camargo, S.E.; Cardoso Jorge, A.O.; de Oliveira, L.D. Thymus vulgaris L. extract has antimicrobial and anti-inflammatory effects in the absence of cy-totoxicity and genotoxicity. Arch. Oral Biol. 2017, 82, 271–279. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sharma, G.; Raturi, K.; Dang, S.; Gupta, S.; Gabrani, R. Inhibitory effect of cinnamaldehyde alone and in combination with thymol, eugenol and thymoquinone against Staphylococcus epidermidis. J. Herb. Med. 2017, 9, 68–73. [Google Scholar] [CrossRef]
- Michalska-Sionkowska, M.; Walczak, M.; Sionkowska, A. Antimicrobial activity of collagen material with thymol addition for potential application as wound dressing. Polym. Test. 2017, 63, 360–366. [Google Scholar] [CrossRef]
- Kachur, K.; Suntres, Z. The antibacterial properties of phenolic isomers, carvacrol and thymol. Crit. Rev. Food Sci. Nutr. 2020, 60, 3042–3053. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Adam, G.; Duncan, H. Development of a sensitive and rapid method for the measurement of total microbial activity using fluorescein diacetate (FDA) in a range of soils. Soil Biol. Biochem. 2001, 33, 943–951. [Google Scholar] [CrossRef] [Green Version]
- Boonruang, K.; Kerddonfag, N.; Chinsirikul, W.; Mitcham, E.J.; Chonhenchob, V. Antifungal effect of poly(lactic acid) films containing thymol and R-(-)-carvone against anthracnose pathogens isolated from avocado and citrus. Food Control. 2017, 78, 85–93. [Google Scholar] [CrossRef]
- Arab, H.-A.; Fathi, M.; Mortezai, E.; Hosseinimehr, S.J. Chemoprotective effect of thymol against genotoxicity induced by bleomycin in human lymphocytes. Pharm. Biomed. Res. 2015, 1, 26–31. [Google Scholar] [CrossRef] [Green Version]
- Palabiyik, S.S.; Karakus, E.; Halici, Z.; Cadirci, E.; Bayir, Y.; Ayaz, G.; Cinar, I. The protective effects of carvacrol and thymol against paracetamol–induced toxicity on human hepatocellular carcinoma cell lines (HepG2). Hum. Exp. Toxicol. 2016, 35, 1252–1263. [Google Scholar] [CrossRef] [PubMed]
- Slamenová, D.; Horváthová, E.; Sramková, M.; Marsálková, L. DNA-protective effects of two components of essential plant oils carvacrol and thymol on mammalian cells cultured in vitro. Neoplasma 2007, 54, 108–112. [Google Scholar]
- Dieser, S.A.; Fessia, A.S.; Ferrari, M.P.; Raspanti, C.G.; Odierno, L.M. Streptococcus uberis: In vitro biofilm production in response to carbohydrates and skim milk. Rev. Argent. Microbiol. 2017, 49, 305–310. [Google Scholar] [CrossRef] [PubMed]
Inhibition Zone Diameter [mm] | ||||||||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Thymol | Carvacrol | Eugenol | Guaiacol | Anethol | ||||||||||||||||
mg/disc | 0.1 | 0.4 | 1 | 4 | 0.1 | 0.4 | 1 | 4 | 0.1 | 0.4 | 1 | 4 | 0.1 | 0.4 | 1 | 4 | 0.1 | 0.4 | 1 | 4 |
S. aureus | 11 | 15 | 17 | 45 | 15 | 29 | 39 | 45 | 0 | 0 | 0 | 16 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
P. aeruginosa | 0 | 11 | 12 | 12 | 0 | 0 | 11 | 11 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
E. coli | 0 | 12 | 18 | 25 | 0 | 12 | 28 | 32 | 0 | 0 | 11 | 21 | 0 | 0 | 0 | 11 | 0 | 0 | 0 | 0 |
C. albicans | 11 | 13 | 18 | 36 | 0 | 12 | 30 | 37 | 0 | 0 | 0 | 23 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
A. niger | 0 | 0 | 11 | 14 | 0 | 0 | 11 | 18 | 0 | 0 | 0 | 11 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
Material | Type | Roughness Ra [mm] | Thickness [mm] |
---|---|---|---|
PP | H | 0.001 | 5 |
PE | 500 | 0.002 | 5 |
PVC | U | 0.003 | 5 |
SS | 304 | 0.002 | 0.2 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Walczak, M.; Michalska-Sionkowska, M.; Olkiewicz, D.; Tarnawska, P.; Warżyńska, O. Potential of Carvacrol and Thymol in Reducing Biofilm Formation on Technical Surfaces. Molecules 2021, 26, 2723. https://doi.org/10.3390/molecules26092723
Walczak M, Michalska-Sionkowska M, Olkiewicz D, Tarnawska P, Warżyńska O. Potential of Carvacrol and Thymol in Reducing Biofilm Formation on Technical Surfaces. Molecules. 2021; 26(9):2723. https://doi.org/10.3390/molecules26092723
Chicago/Turabian StyleWalczak, Maciej, Marta Michalska-Sionkowska, Daria Olkiewicz, Patrycja Tarnawska, and Oliwia Warżyńska. 2021. "Potential of Carvacrol and Thymol in Reducing Biofilm Formation on Technical Surfaces" Molecules 26, no. 9: 2723. https://doi.org/10.3390/molecules26092723