Generic placeholder image

Current Pharmaceutical Biotechnology

Editor-in-Chief

ISSN (Print): 1389-2010
ISSN (Online): 1873-4316

Research Article

Investigation on the Antibacterial Activity of Electronic Cigarette Liquids (ECLs): A Proof of Concept Study

Author(s): Virginia Fuochi, Massimo Caruso , Rosalia Emma, Aldo Stivala, Riccardo Polosa, Alfio Distefano and Pio M. Furneri *

Volume 22, Issue 7, 2021

Published on: 03 September, 2020

Page: [983 - 994] Pages: 12

DOI: 10.2174/1389201021666200903121624

open access plus

Abstract

Background: The key ingredients of e-cigarettes liquid are commonly propane-1,2-diol (also called propylene glycol) and propane-1,2,3-triol (vegetal glycerol) and their antimicrobial effects are already established. The nicotine and flavors which are often present in e-liquids can interfere with the growth of some microorganisms. Objective: The effect of combining these elements in e-liquids is unknown. The aim of the study was to investigate the possible effects of these liquids on bacterial growth in the presence or absence of nicotine and flavors.

Methods: Susceptibilities of pathogenic strains (Klebsiella pneumoniae, Staphylococcus aureus, Pseudomonas aeruginosa, Acinetobacter baumannii, Escherichia coli, Enterococcus faecalis and Sarcina lutea) were studied by means of a multidisciplinary approach. Cell viability and antioxidant assays were also evaluated.

Results: All e-liquids investigated showed antibacterial activity against at least one pathogenic strain. Higher activity was correlated to the presence of flavors and nicotine.

Discussion: In most cases, the value of minimal bactericidal concentration is equal to the value of minimal inhibitory concentration showing that these substances have a bactericidal effect. This effect was observed in concentrations up to 6.25% v/v. Antioxidant activity was also correlated to the presence of flavors. Over time, the viability assay in human epithelial lung A549 cells showed a dose-dependent inhibition of cell growth.

Conclusion: Our results have shown that flavors considerably enhance the antibacterial activity of propane-1,2-diol and propane-1,2,3-triol. This study provides important evidence that should be taken into consideration in further investigative approaches, to clarify the different sensitivity of the various bacterial species to e-liquids, including the respiratory microbiota, to highlight the possible role of flavors and nicotine.

Keywords: Electronic cigarettes, e-liquids, flavors, nicotine, propane-1, 2-diol, propane-1, 2, 3-triol, antibacterial activity.

« Previous
Graphical Abstract

[1]
Roger, V.; Fonty, G.; Andre, C.; Gouet, P. Effects of glycerol on the growth, adhesion, and cellulolytic activity of rumen cellulolytic bacteria and anaerobic fungi. Curr. Microbiol., 1992, 25(4), 197-201.
[http://dx.doi.org/10.1007/BF01570719] [PMID: 1368974]
[2]
Kinyoun, J.J. The action of glycerin on bacteria in the presence of cell exudates. J. Exp. Med., 1905, 7(6), 725-732.
[http://dx.doi.org/10.1084/jem.7.6.725] [PMID: 19867018]
[3]
Farsalinos, K.; Cibella, F.; Caponnetto, P.; Campagna, D.; Morjaria, J.B.; Battaglia, E.; Caruso, M.; Russo, C.; Polosa, R. Effect of continuous smoking reduction and abstinence on blood pressure and heart rate in smokers switching to electronic cigarettes. Intern. Emerg. Med., 2016, 11(1), 85-94.
[http://dx.doi.org/10.1007/s11739-015-1361-y] [PMID: 26749533]
[4]
Polosa, R.; Rodu, B.; Caponnetto, P.; Maglia, M.; Raciti, C. A fresh look at tobacco harm reduction: The case for the electronic cigarette. Harm Reduction Journal, 2013, 10(19)
[http://dx.doi.org/10.1186/1477-7517-10-19]
[5]
Robertson, O.H.; Bigg, E.; Puck, T.T.; Miller, B.F. Technical Assistance of Elizabeth A. Appell. Technical Assistance of Elizabeth, A.A. The bactericidal action of propylene glycol vapor on microorganisms suspended in air. I. J. Exp. Med., 1942, 75(6), 593-610.
[http://dx.doi.org/10.1084/jem.75.6.593] [PMID: 19871209]
[6]
Olitzky, I.; Mattly, K.G. Special purpose culture media containing propylene glycol. Appl. Microbiol., 1967, 15(1), 205.
[http://dx.doi.org/10.1128/AEM.15.1.205-.1967] [PMID: 6031438]
[7]
Robertson, O.H.; Loosli, C.G.; Puck, T.T.; Bigg, E.; Miller, B.F. The protection of mice against infection with air-borne influenza virus by means of propylene glycol vapor. Science, 1941, 94(2452), 612-613.
[http://dx.doi.org/10.1126/science.94.2452.612] [PMID: 17740060]
[8]
Abdelmonem, R.; Younis, M.K.; Hassan, D.H.; El-Sayed Ahmed, M.A.E.; Hassanein, E.; El-Batouty, K.; Elfaham, A. Formulation and characterization of chlorhexidine HCl nanoemulsion as a promising antibacterial root canal irrigant: in-vitro and ex-vivo studies. Int. J. Nanomedicine, 2019, 14, 4697-4708.
[http://dx.doi.org/10.2147/IJN.S204550] [PMID: 31303754]
[9]
Vanić, Ž.; Rukavina, Z.; Manner, S.; Fallarero, A.; Uzelac, L.; Kralj, M.; Amidžić Klarić, D.; Bogdanov, A.; Raffai, T.; Virok, D.P.; Filipović-Grčić, J.; Škalko-Basnet, N. Azithromycin-liposomes as a novel approach for localized therapy of cervicovaginal bacterial infections. Int. J. Nanomedicine, 2019, 14, 5957-5976.
[http://dx.doi.org/10.2147/IJN.S211691] [PMID: 31440052]
[10]
Yi, L.; Tian, M.; Piao, C.; Gao, G.; Wu, L.; Pan, Y.; Liu, J. The protective effects of 1,2-propanediol against radiation-induced hematopoietic injury in mice. Biomed. Pharmacother., 2019, 114, 108806.
[http://dx.doi.org/10.1016/j.biopha.2019.108806] [PMID: 30928804]
[11]
Stout, E.I.; McKessor, A. Glycerin-based hydrogel for infection control. Adv. Wound Care (New Rochelle), 2012, 1(1), 48-51.
[http://dx.doi.org/10.1089/wound.2011.0288] [PMID: 24527279]
[12]
Manconi, M.; Petretto, G.; D’hallewin, G.; Escribano, E.; Milia, E.; Pinna, R.; Palmieri, A.; Firoznezhad, M.; Peris, J.E.; Usach, I.; Fadda, A.M.; Caddeo, C.; Manca, M.L. Thymus essential oil extraction, characterization and incorporation in phospholipid vesicles for the antioxidant/antibacterial treatment of oral cavity diseases. Colloids Surf. B Biointerfaces, 2018, 171, 115-122.
[http://dx.doi.org/10.1016/j.colsurfb.2018.07.021] [PMID: 30025373]
[13]
Pavia, C.S.; Pierre, A.; Nowakowski, J. Antimicrobial activity of nicotine against a spectrum of bacterial and fungal pathogens. J. Med. Microbiol., 2000, 49(7), 675-676.
[http://dx.doi.org/10.1099/0022-1317-49-7-675] [PMID: 10882095]
[14]
Gandhi, P.T.; Athmaram, T.N.; Arunkumar, G.R. Novel nicotine analogues with potential anti-mycobacterial activity. Bioorg. Med. Chem., 2016, 24(8), 1637-1647.
[http://dx.doi.org/10.1016/j.bmc.2016.02.035] [PMID: 26951892]
[15]
Salman, S.; Idrees, F.; Pervaiz, S.; Shah, F.H.; Badshah, S.; Abdullah, ; Usman, M.; Halimi, S.A.; Idrees, J. Short communication: evaluation of antimicrobial activities of harmine, harmaline, nicotine and their complexes. Pak. J. Pharm. Sci., 2016, 29(4), 1317-1320.
[PMID: 27393444]
[16]
F.D.A.. U.S. CFR - Code of Federal Regulations Title 21 FOOD AND DRUGS; Food and Drug Administration: 10903 New Hampshire Avenue Silver Spring, MD 20993 2019, 500-559.
[17]
Russell, C.; McKeganey, N.; Dickson, T.; Nides, M. Changing patterns of first e-cigarette flavor used and current flavors used by 20,836 adult frequent e-cigarette users in the USA. Harm Reduction J., 2018.
[18]
Furneri, P.M.; Fuochi, V.; Lissandrello, E.; Petronio Petronio, G.; Fresta, M.; Paolino, D. In Frontiers in Anti-Infective Drug Discovery. Bentham Science Publishers, 2017, 5, 23-54.
[19]
Puglia, C.; Pignatello, R.; Fuochi, V.; Furneri, P.M.; Lauro, M.R.; Santonocito, D.; Cortesi, R.; Esposito, E. Lipid nanoparticles and active natural compounds: A perfect combination for pharmaceutical applications. Curr. Med. Chem., 2019, 26(24), 4681-4696.
[http://dx.doi.org/10.2174/0929867326666190614123835] [PMID: 31203795]
[20]
Kavanagh, F. Analytical Microbiology; ACADEMIC PRESS INC.: 111 Fifth Avenue, New York 3, New York, 1972.
[21]
Kavanagh, F. Analytical Microbiology; ACADEMIC PRESS INC.: l l Fifth Avenue, New York 3, New York, 1963.
[22]
Fuochi, V.; Volti, G.L.; Furneri, P.M. Probiotic properties of lactobacillus fermentum strains isolated from human oral samples and description of their antibacterial activity. Curr. Pharm. Biotechnol., 2017, 18(2), 138-149.
[http://dx.doi.org/10.2174/1389201017666161229153530] [PMID: 28034294]
[23]
C.L.S.I. M100 S29 Performance Standards for Antimicrobial Susceptibility Testing Clinical Laboratory Standards Institute: 950 West Valley Road, Suite 2500, Wayne, Pennsylvania 19087 USA 2019.
[24]
Fuochi, V.; Li Volti, G.; Camiolo, G.; Tiralongo, F.; Giallongo, C.; Distefano, A.; Petronio Petronio, G.; Barbagallo, I.; Viola, M.; Furneri, P.M.; Di Rosa, M.; Avola, R.; Tibullo, D. Antimicrobial and anti-proliferative effects of skin mucus derived from Dasyatis pastinaca (Linnaeus, 1758). Mar. Drugs, 2017, 15(11), E342.
[http://dx.doi.org/10.3390/md15110342] [PMID: 29104260]
[25]
Fuochi, V.; Cardile, V.; Petronio Petronio, G.; Furneri, P.M. Biological properties and production of bacteriocins-like-inhibitory substances by Lactobacillus sp. strains from human vagina. J. Appl. Microbiol., 2018.
[http://dx.doi.org/10.1111/jam.14164] [PMID: 30499608]
[26]
MicrochemLaboratory Minimum Bactericidal Concentration (MBC) Test. http://microchemlab.com/test/minimum-bactericidal-concentration-mbc-test
[27]
Bueno, J. Models of evaluation of antimicrobial activity of essential oils in vapour phase: A promising use in healthcare decontamination. Nat. Volatiles Essent. Oils, 2015, 2(2), 16-29.
[28]
Inouye, S.; Uchida, K.; Maruyama, N.; Yamaguchi, H.; Abe, S. A novel method to estimate the contribution of the vapor activity of essential oils in agar diffusion assay. Nippon Ishinkin Gakkai Zasshi, 2006, 47(2), 91-98.
[http://dx.doi.org/10.3314/jjmm.47.91] [PMID: 16699489]
[29]
Fuochi, V.; Petronio, G.P.; Lissandrello, E.; Furneri, P.M. Evaluation of resistance to low pH and bile salts of human Lactobacillus spp. isolates. Int. J. Immunopathol. Pharmacol., 2015, 28(3), 426-433.
[http://dx.doi.org/10.1177/0394632015590948] [PMID: 26216909]
[30]
Fuochi, V.; Barbagallo, I.; Distefano, A.; Puglisi, F.; Palmeri, R.; Di Rosa, M.; Giallongo, C.; Longhitano, L.; Fontana, P.; Sferrazzo, G.; Tiralongo, F.; Raccuia, S.A.; Ronsisvalle, S.; Li Volti, G.; Furneri, P.M.; Tibullo, D. Biological properties of Cakile maritima Scop. (Brassicaceae) extracts. Eur. Rev. Med. Pharmacol. Sci., 2019, 23(5), 2280-2292.
[http://dx.doi.org/10.26355/eurrev_201903_17277] [PMID: 30915777]
[31]
Kinnunen, T.; Koskela, M. Antibacterial and antifungal properties of propylene glycol, hexylene glycol, and 1,3-butylene glycol in vitro. Acta Derm. Venereol., 1991, 71(2), 148-150.
[PMID: 1675525]
[32]
Gudmundsson, S.; Vogelman, B.; Craig, W.A. Decreased bactericidal activity during the period of the postantibiotic effect. J. Antimicrob. Chemother., 1994, 34(6), 921-930.
[http://dx.doi.org/10.1093/jac/34.6.921] [PMID: 7730235]
[33]
Hozumi, H.; Hasegawa, S.; Tsunenari, T.; Sanpei, N.; Arashina, Y.; Takahashi, K.; Konnno, A.; Chida, E.; Tomimatsu, S. Aromatherapies using Osmanthus fragrans oil and grapefruit oil are effective complementary treatments for anxious patients undergoing colonoscopy: A randomized controlled study. Complement. Ther. Med., 2017, 34, 165-169.
[http://dx.doi.org/10.1016/j.ctim.2017.08.012] [PMID: 28917370]
[34]
Furneri, P.M.; Mondello, L.; Mandalari, G.; Paolino, D.; Dugo, P.; Garozzo, A.; Bisignano, G. In vitro antimycoplasmal activity of Citrus bergamia essential oil and its major components. Eur. J. Med. Chem., 2012, 52, 66-69.
[http://dx.doi.org/10.1016/j.ejmech.2012.03.005] [PMID: 22465092]
[35]
Pattnaik, S.; Subramanyam, V.R.; Bapaji, M.; Kole, C.R. Antibacterial and antifungal activity of aromatic constituents of essential oils. Microbios, 1997, 89(358), 39-46.
[PMID: 9218354]
[36]
Kifer, D.; Mužinić, V.; Klarić, M.S. Antimicrobial potency of single and combined mupirocin and monoterpenes, thymol, menthol and 1,8-cineole against Staphylococcus aureus planktonic and biofilm growth. J. Antibiot. (Tokyo), 2016, 69(9), 689-696.
[http://dx.doi.org/10.1038/ja.2016.10] [PMID: 26883392]
[37]
Huang, J.; Qian, C.; Xu, H.; Huang, Y. Antibacterial activity of Artemisia asiatica essential oil against some common respiratory infection causing bacterial strains and its mechanism of action in Haemophilus influenzae. Microb. Pathog., 2018, 114, 470-475.
[http://dx.doi.org/10.1016/j.micpath.2017.12.032] [PMID: 29241769]
[38]
Cowan, M.M. Plant products as antimicrobial agents. Clin. Microbiol. Rev., 1999, 12(4), 564-582.
[http://dx.doi.org/10.1128/CMR.12.4.564] [PMID: 10515903]
[39]
Roshan, N.; Riley, T.V.; Knight, D.R.; Steer, J.H.; Hammer, K.A. Natural products show diverse mechanisms of action against Clostridium difficile. J. Appl. Microbiol., 2019, 126(2), 468-479.
[http://dx.doi.org/10.1111/jam.14152] [PMID: 30412324]
[40]
Hendry, E.R.; Worthington, T.; Conway, B.R.; Lambert, P.A. Antimicrobial efficacy of eucalyptus oil and 1,8-cineole alone and in combination with chlorhexidine digluconate against microorganisms grown in planktonic and biofilm cultures. J. Antimicrob. Chemother., 2009, 64(6), 1219-1225.
[http://dx.doi.org/10.1093/jac/dkp362] [PMID: 19837714]
[41]
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., 2005, 49(6), 2474-2478.
[http://dx.doi.org/10.1128/AAC.49.6.2474-2478.2005] [PMID: 15917549]
[42]
Bezerra, C.F.; Camilo, C.J.; do Nascimento Silva, M.K.; de Freitas, T.S.; Ribeiro-Filho, J.; Coutinho, H.D.M. Vanillin selectively modulates the action of antibiotics against resistant bacteria. Microb. Pathog., 2017, 113, 265-268.
[http://dx.doi.org/10.1016/j.micpath.2017.10.052] [PMID: 29107747]
[43]
Kwiatkowski, P.; Pruss, A.; Wojciuk, B.; Dołęgowska, B.; Wajs-Bonikowska, A.; Sienkiewicz, M.; Mężyńska, M.; Łopusiewicz, Ł. The influence of essential oil compounds on antibacterial activity of mupirocin-susceptible and induced low-level mupirocin-Resistant MRSA Strains. Molecules, 2019, 24(17), E3105.
[http://dx.doi.org/10.3390/molecules24173105] [PMID: 31461850]
[44]
Hançer Aydemir, D.; Çifci, G.; Aviyente, V.; Boşgelmez-Tinaz, G. Quorum-sensing inhibitor potential of trans-anethole aganist Pseudomonas aeruginosa. J. Appl. Microbiol., 2018, 125(3), 731-739.
[http://dx.doi.org/10.1111/jam.13892] [PMID: 29694695]
[45]
Auezova, L.; Najjar, A.; Kfoury, M.; Fourmentin, S.; Greige-Gerges, H. Antibacterial activity of free or encapsulated selected phenylpropanoids against Escherichia coli and Staphylococcus epidermidis. J. Appl. Microbiol., 2019.
[http://dx.doi.org/10.1111/jam.14516] [PMID: 31710756]
[46]
Trombetta, D.; Cimino, F.; Cristani, M.; Mandalari, G.; Saija, A.; Ginestra, G.; Speciale, A.; Chirafisi, J.; Bisignano, G.; Waldron, K.; Narbad, A.; Faulds, C.B. In vitro protective effects of two extracts from bergamot peels on human endothelial cells exposed to tumor necrosis factor-alpha (TNF-alpha). J. Agric. Food Chem., 2010, 58(14), 8430-8436.
[http://dx.doi.org/10.1021/jf1008605] [PMID: 20578719]
[47]
Postu, P.A.; Sadiki, F.Z.; El Idrissi, M.; Cioanca, O.; Trifan, A.; Hancianu, M.; Hritcu, L. Pinus halepensis essential oil attenuates the toxic Alzheimer’s amyloid beta (1-42)-induced memory impairment and oxidative stress in the rat hippocampus. Biomed. Pharmacother., 2019, 112, 108673.
[http://dx.doi.org/10.1016/j.biopha.2019.108673] [PMID: 30784941]
[48]
Agatonovic-Kustrin, S.; Kustrin, E.; Morton, D.W. Essential oils and functional herbs for healthy aging. Neural Regen. Res., 2019, 14(3), 441-445.
[http://dx.doi.org/10.4103/1673-5374.245467] [PMID: 30539810]
[49]
Aponso, M.; Patti, A.; Bennett, L.E. Dose-related effects of inhaled essential oils on behavioural measures of anxiety and depression and biomarkers of oxidative stress. J. Ethnopharmacol., 2020, 250, 112469.
[http://dx.doi.org/10.1016/j.jep.2019.112469] [PMID: 31843574]
[50]
Subhadradevi, V.; Asokkumar, K.; Umamaheswari, M.; Sivashanmugam, A.; Sankaranand, R. In vitro antioxidant activity of Vetiveria Zizanioides root extract. Tanzan. J. Health Res., 2010, 12(4), 274-279.
[http://dx.doi.org/10.4314/thrb.v12i4.59314] [PMID: 24409635]
[51]
Mohamed, A.; Afridi, D.M.; Garani, O.; Tucci, M. Thymoquinone inhibits the activation of NF-kappaB in the brain and spinal cord of experimental autoimmune encephalomyelitis. Biomed. Sci. Instrum., 2005, 41, 388-393.
[PMID: 15850137]
[52]
Mohamed, A.; Shoker, A.; Bendjelloul, F.; Mare, A.; Alzrigh, M.; Benghuzzi, H.; Desin, T. Improvement of experimental allergic encephalomyelitis (EAE) by thymoquinone; an oxidative stress inhibitor. Biomed. Sci. Instrum., 2003, 39, 440-445.
[PMID: 12724933]
[53]
Behar, R.Z.; Wang, Y.; Talbot, P. Comparing the cytotoxicity of electronic cigarette fluids, aerosols and solvents. Tob. Control, 2018, 27(3), 325-333.
[http://dx.doi.org/10.1136/tobaccocontrol-2016-053472] [PMID: 28596276]
[54]
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(5), 565-573.
[http://dx.doi.org/10.1093/jac/47.5.565] [PMID: 11328766]
[55]
EUCAST. In Breakpoint tables for interpretation of MICs and zone diameters; , 2020.

© 2024 Bentham Science Publishers | Privacy Policy