Antibacterial activity of cinnamon oil against multidrug-resistant Salmonellaserotypes and anti-quorum sensing potential

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Published: Jan 21, 2023
Updated: 2023-01-21
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2023-01-21 (2)
DOI: https://doi.org/10.12681/jhvms.25514
Keywords:
antibacterial activity anti-quorum sensing activity cinnamon oil multidrug resistant Salmonella enterica
Merve Eylul Kiymaci
University of Health Sciences Turkey
https://orcid.org/0000-0001-5343-1064
Banu Kaskatepe
Ankara University
https://orcid.org/0000-0002-9722-4267
Yesim Soyer
Middle East Technical University
https://orcid.org/0000-0001-9687-9715
Abstract

The antimicrobial resistance due to Salmonella and other foodborne pathogenic microorganisms, witnessed in recent years, has become a significant health concern. Bacteria use chemical signals to communicate each other and regulate their behavior including virulence. Depending increased antibiotic resistance, new drug development strategies being investigating and the usability of active ingredients of various medicinal and aromatic plants is especially tested as an alternative. The aim of this study was to determine the anti-quorum sensing (QS) activity of cinnamon oil (CO) on pigment production of Chromobacterium violaceum and to evaluate antibacterial activity against multidrug resistant (MDR) S. enterica serotypes. Anti QS activity was tested using biosensor strain and antibacterial activity was determined by microdilution method according to EUCAST standards. CO was found effective on QS mechanisms of Chromobacterium violaceum with pigment inhibition. Nineteen foodborne pathogens isolated from different poultry/cow sourced foods and serotyped as S. enterica serovar Infantis (15), Kentucky (1), Newport (1), Telaviv (1), and Typhimurium (1). S. enterica Infantis strains were found resistant to three or more antibiotics and categorized as MDR. The results concluded that CO has strong antibacterial activity against all S. enterica serotypes with MIC between 0.125 µg ml-1 and 1.0 µg ml-1. This research demonstrates CO is a potential candidate for developing new antimicrobial agents, antiseptic solutions or natural food preservatives against MDR Salmonella isolates also a potential as an anti-QS agent.

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References
Acar S, Bulut E, Durul B, et al. (2017) Phenotyping and genetic characterization of Salmonella enterica isolates from Turkey revealing arise of different features specific to geography. Int J Food Microbiol 241:98-107 doi:10.1016/j.ijfoodmicro.2016.09.031
Akthar M, Degaga, B., & Azam, T. (2014) Antimicrobial activity of essential oils extracted from medicinal plants against the pathogenic microorganisms: a review. Issues in Biological Sciences and Pharmaceutical Research 2(1):1-7
Alibi S, Ben Selma W, Ramos-Vivas J, et al. (2020) Anti-oxidant, antibacterial, anti-biofilm, and anti-quorum sensing activities of four essential oils against multidrug-resistant bacterial clinical isolates. Curr Res Transl Med 68(2):59-66 doi:10.1016/j.retram.2020.01.001
Almeida F, Pitondo-Silva A, Oliveira MA, Falcao JP (2013) Molecular epidemiology and virulence markers of Salmonella Infantis isolated over 25 years in Sao Paulo State, Brazil. Infect Genet Evol 19:145-151 doi:10.1016/j.meegid.2013.07.004
Aminov RI (2010) A brief history of the antibiotic era: lessons learned and challenges for the future. Front Microbiol 1:134 doi:10.3389/fmicb.2010.00134
Anwar F, Hussain AI, Sherazi STH, Bhanger MI (2009) Changes incomposition and antioxidant and antimicrobial activities of essential oil offennel (Foeniculum vulgare Mill.) fruit at different stages of maturity. J HerbsSpices Med Plants 15:1-16
Arumugam G, Swamy MK, Sinniah UR (2016) Plectranthus amboinicus (Lour.) Spreng: Botanical, Phytochemical, Pharmacological and Nutritional Significance. Molecules 21(4):369 doi:10.3390/molecules21040369
Bagheri L, Khodaei, N., Salmieri, S., Karboune, S., Lacroix, M. (2020) Correlation between chemical composition and antimicrobial properties of essential oils against most common food pathogens and spoilers: In-vitro efficacy and predictive modelling. Microbial pathogenesis 147, 104212 doi:https://doi.org/10.1016/j.micpath.2020.104212
Brnawi WI, Hettiarachchy NS, Horax R, Kumar-Phillips G, Seo HS, Marcy J (2018) Comparison of Cinnamon Essential Oils from Leaf and Bark with Respect to Antimicrobial Activity and Sensory Acceptability in Strawberry Shake. J Food Sci 83(2):475-480 doi:10.1111/1750-3841.14041
Burt S (2004) Essential oils: their antibacterial properties and potential applications in foods--a review. Int J Food Microbiol 94(3):223-53 doi:10.1016/j.ijfoodmicro.2004.03.022
CDC (2018) (Centers for Disease Control and Prevention) Salmonella. https://www.cdc.gov/salmonella/general/index.html (accessed 10 september 2018).
Chen CH, Ravishankar S, Marchello J, Friedman M (2013) Antimicrobial Activity of Plant Compounds against Salmonella Typhimurium DT104 in Ground Pork and the Influence of Heat and Storage on the Antimicrobial Activity. J Food Protect 76(7):1264-1269 doi:10.4315/0362-028x.Jfp-12-493
Chuesiang P, Siripatrawan, U., Sanguandeekul, R., Yang, J.S., McClements, D.J., McLandsborough, L. (2019) Antimicrobial activity and chemical stability of cinnamon oil in oil-in-water nanoemulsions fabricated using the phase inversion temperature method. LWT 110:190-196 doi:10.1016/j.lwt.2019.03.012
CLSI (2012) Performance Standards for Antimicrobial Susceptibility Testing; 22nd In- formational Supplement, M100-S22. Clinical and Laboratory Standards Institute, Wayne, PA.
Domínguez-Borbor C, Sánchez-Rodríguez, A., Sonnenholzner, S., Rodríguez, J. (2020) Essential oils mediated antivirulence therapy against vibriosis in Penaeus vannamei. Aquaculture 529, 735639
Durul B, Acar S, Bulut E, Kyere EO, Soyer Y (2015) Subtyping of Salmonella Food Isolates Suggests the Geographic Clustering of Serotype Telaviv. Foodborne Pathog Dis 12(12):958-65 doi:10.1089/fpd.2015.1995
ECDC (2016) The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2014. EFSA J 14 doi:438010.2903/j.efsa.2016.4380
Erdonmez D, Rad AY, Aksoz N (2018) Anti-Quorum Sensing Potential of Antioxidant Quercetin and Resveratrol. Braz Arch Biol Techn 61
EUCAST (2016) Breakpoint tables for interpretation of MICs and zone diameters, Version 6.0.
European Committee on Antimicrobial Susceptibility Testing. http://www.eucast.org. (accesed 10 June 2016).
Foley SL, Lynne AM (2008) Food animal-associated Salmonella challenges: pathogenicity and antimicrobial resistance. J Anim Sci 86(14 Suppl):E173-87 doi:10.2527/jas.2007-0447
Grimont P, Weil F (2007) Antigenic Formulae of the Salmonella Servovars. 9th ed. Pas-teur Institute, Paris (World Health Organization Centre for Reference and Researchon Salmonella).
Haddi K, Faroni LRA, Oliveira EE (2017) Cinnamon oil: Green Pesticides Handbook. In book: Green Pesticides Handbook Essential Oils for Pest ControlEdition: 1Chapter: 7Publisher: CRC Press Taylor & Francis GroupEditors: Leo M.L. Nollet, Hamir Singh Rathore. p-118-138.
JakarwanYostawonkula NN, Atitaya Phasuk, Rachatapan Junchay, Suwimon Boonrungsiman, Sasithon Temisak, Mesayamas Kongsema, Waranyoo Phoolcharoen, Teerapong Yata (2021) Nano/microstructured hybrid composite particles containing cinnamon oil as an antibiotic alternative against food-borne pathogens. Journal of Food Engineering 290, 110209 doi:https://doi.org/10.1016/j.jfoodeng.2020.110209
Kalia M, Yadav VK, Singh PK, et al. (2015) Effect of Cinnamon Oil on Quorum Sensing-Controlled Virulence Factors and Biofilm Formation in Pseudomonas aeruginosa. Plos One 10(8) doi:ARTN e0135495
1371/journal.pone.0135495
Kaskatepe B, Kiymaci, M. E., Simsek, D., Erol, H. B., & Erdem, S. A. (2016) Comparison of the contents and antimicrobial activities of commercial and natural cinnamon oils. Indian Journal of Pharmaceutical Sciences 78(4) doi:10.4172/pharmaceutical-sciences.1000150
Kavyani B, Arabestani MR, Nejad ASM, et al. (2019) The Effect of Cinnamon Bark on the Expression of Quorum Sensing System and Virulence Genes in Pseudomonas aeruginosa Strain PAO1. Res J Biotechnol 14(2):42-48
Kiymaci ME, Altanlar N, Gumustas M, Ozkan SA, Akin A (2018) Quorum sensing signals and related virulence inhibition of Pseudomonas aeruginosa by a potential probiotic strain's organic acid. Microb Pathog 121:190-197 doi:10.1016/j.micpath.2018.05.042
Li SZ, Zhou JY, Wang YN, et al. (2019) Physicochemical and Antimicrobial Properties of Hydroxypropyl Methylcellulose-Cinnamon Essential Oil Emulsion: Effects of Micro- and Nanodroplets. Int J Food Eng 15(9) doi:ARTN 20180416
1515/ijfe-2018-0416
Majowicz SE, Musto J, Scallan E, et al. (2010) The Global Burden of Nontyphoidal Salmonella Gastroenteritis. Clin Infect Dis 50(6):882-889 doi:10.1086/650733
McClean KH, Winson MK, Fish L, et al. (1997) Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology 143 ( Pt 12):3703-11 doi:10.1099/00221287-143-12-3703
McEwen SA, Fedorka-Cray PJ (2002) Antimicrobial use and resistance in animals. Clin Infect Dis 34:S93-S106 doi:Doi 10.1086/340246
Medalla F, Gu WD, Mahon BE, et al. (2017) Estimated Incidence of Antimicrobial Drug-Resistant Nontyphoidal Salmonella Infections, United States, 2004-2012. Emerg Infect Dis 23(1):29-37 doi:10.3201/eid2301.160771
Papenfort K, Bassler BL (2016) Quorum sensing signal-response systems in Gram-negative bacteria. Nat Rev Microbiol 14(9):576-88 doi:10.1038/nrmicro.2016.89
Paudel SK, Bhargava, K., Kotturi, H. (2019) Antimicrobial activity of cinnamon oil nanoemulsion against Listeria monocytogenes and Salmonella spp. on melons. LWT 111:682-687 doi:10.1016/j.lwt.2019.05.087
Piovezan M, Uchida NS, da Silva AF, et al. (2014) Effect of cinnamon essential oil and cinnamaldehyde on Salmonella Saintpaul biofilm on a stainless steel surface. J Gen Appl Microbiol 60(3):119-121 doi:10.2323/jgam.60.119
Ranjbar R, Sarshar M, Sadeghifard N (2012) Characterization of genetic diversity among clinical strains of Salmonella enterica serovar Infantis by ribotyping method. Sci J Zanjan 20:75–84
Rasko DA, Sperandio V (2010) Anti-virulence strategies to combat bacteria-mediated disease. Nat Rev Drug Discov 9(2):117-28 doi:10.1038/nrd3013
Soyer Y, Richards J, Hoelzer K, et al. (2013) Antimicrobial Drug Resistance Patterns among Cattle- and Human-Associated Salmonella Strains. J Food Protect 76(10):1676-1688 doi:10.4315/0362-028x.Jfp-13-018
Swamy KM, Neeki, M. A., Bhaumik, S. H., Darshil, S. H., Vijay, R., & Kashyap, S. (2012) Phytochemical screening and in vitro antimicrobial activity of Bougainvillea spectabilis flower extracts. International Journal of Phytomedicine 4(3):375–379
Swamy MK, Sinniah UR (2015) A Comprehensive Review on the Phytochemical Constituents and Pharmacological Activities of Pogostemon cablin Benth.: An Aromatic Medicinal Plant of Industrial Importance. Molecules 20(5):8521-47 doi:10.3390/molecules20058521
Todd J, Friedman M, Patel J, Jaroni D, Ravishankar S (2013) The antimicrobial effects of cinnamon leaf oil against multi-drug resistant Salmonella Newport on organic leafy greens. Int J Food Microbiol 166(1):193-199 doi:10.1016/j.ijfoodmicro.2013.06.021
Upadhyaya I, Upadhyay A, Kollanoor-Johny A, et al. (2015) In-Feed Supplementation of trans-Cinnamaldehyde Reduces Layer-Chicken Egg-Borne Transmission of Salmonella enterica Serovar Enteritidis. Appl Environ Microb 81(9):2985-2994 doi:10.1128/Aem.03809-14
Vasconcelos NG, Croda J, Simionatto S (2018) Antibacterial mechanisms of cinnamon and its constituents: A review. Microb Pathog 120:198-203 doi:10.1016/j.micpath.2018.04.036
Waters V, Smyth A (2015) Cystic fibrosis microbiology: Advances in antimicrobial therapy. J Cyst Fibros 14(5):551-60 doi:10.1016/j.jcf.2015.02.005
WHO (2018) Salmonella (non-typhoidal) http://www.who.int/news-room/fact-sheets/detail/salmonella-(non-typhoidal) (accessed 15 Agust 2018).