Therapeutic Effect of Zataria Multiflora Essential Oil on Burn Wound Infected by Pseudomonas aeruginosa

Document Type : Original Article

Authors

1 Student Research Committee, Shiraz University of Medical Sciences, Shiraz, Iran

2 Department of Biochemistry, Microbiology and Immunology, University of Ottawa, Ottawa, Canada

3 Department of Pharmacology, School of Medicine, Shiraz University of Medical Sciences, Shiraz, Iran

4 Cardiovascular Research Center, Shiraz University of Medical Sciences, Shiraz, Iran

5 Department of Medical Laboratory Sciences, School of Paramedical Sciences, Shiraz University of Medical Sciences, Shiraz, Iran

6 Department of Pathology, Shiraz University of Medical Sciences, Shiraz, Iran

7 Central Research Laboratory, Shiraz University of Medical Sciences, Shiraz, Iran

10.30476/tips.2024.103860.1254

Abstract

Pseudomonas aeruginosa (P. aeruginosa) is one of the most important microorganisms causing burn wound infection. Due to the rapid increase in resistance to the currently used antimicrobial agents, finding new antibiotics is one of the research priorities. This study was designed to investigate antibacterial and wound healing effects of Zataria multiflora essential oil (ZMEO) on burn wounds infected with P. aeruginosa in Sprague-Dawley rats. Experimental burn wounds were created on the back of the animals and infected with P. aeruginosa. The animals were randomly divided into 4 groups of 7 to 10 as follow: negative control (no treatment), carrier gel group treated with carboxymethyl cellulose (CMC) gel, ZMEO group that received CMC gel loaded with ZMEO, and positive control group that received silver sulfadiazine (SSD). All medications were applied topically once daily for 28 days. On the days 7th, 14th, 21st, and 28th after the start of treatments, the surfaces of the wounds were measured and some samples were collected for histopathological evaluations. The tensile strengths of ratsʼ skins were also measured on the 28th day. The results showed that on the 7th day, while a significant healing of the wounds was observed in the ZMEO group, the other groups did not show remarkable wound healing (P<0.05). Therefore, ZMEO showed an accelerating effect on the healing process of burn wounds and could be considered for further evaluations in order to develop new medications for the treatment of burn wounds infected with P. aeruginosa. 

Highlights

Elahe Sattarrinezhad (Google Scholar)

Maryam Motevasel (Google Scholar)

Keywords


1.    Hashemi SS, Sharhani A, Lotfi B, Ahmadi-Juibari T, Shaahmadi Z, Aghaei A. A Systematic Review on the Epidemiology of Pediatric Burn in Iran. J Burn Care Res. 2017 Nov/Dec;38(6):e944-e951. doi: 10.1097/BCR.0000000000000524. Erratum in: J Burn Care Res. 2018 Jan 1;39(1):173. doi: 10.1093/jbcr/irx059. PMID: 28328658.
2.    Church D, Elsayed S, Reid O, Winston B, Lindsay R. Burn wound infections. Clin Microbiol Rev. 2006 Apr;19(2):403-34. doi: 10.1128/CMR.19.2.403-434.2006. PMID: 16614255; PMCID: PMC1471990.
3.    Rajput A, Saxena R, Singh KP, Kumar V, Singh S, Gupta A, Singh RK. Prevalence and antibiotic resistance pattern of metallo-beta-lactamase-producing Pseudomonas aeruginosa from burn patients--experience of an Indian tertiary care hospital. J Burn Care Res. 2010 Mar-Apr;31(2):264-8. doi: 10.1097/BCR.0b013e3181d0f4bf. PMID: 20182377.
4.    Nikokar I, Tishayar A, Flakiyan Z, Alijani K, Rehana-Banisaeed S, Hossinpour M, Amir-Alvaei S, Araghian A. Antibiotic resistance and frequency of class 1 integrons among Pseudomonas aeruginosa, isolated from burn patients in Guilan, Iran. Iran J Microbiol. 2013 Mar;5(1):36-41. PMID: 23466812; PMCID: PMC3577559.
5.    De Luca I, Pedram P, Moeini A, Cerruti P, Peluso G, Di Salle A, et al. Nanotechnology development for formulating essential oils in wound dressing materials to promote the wound-healing process: a review. Appl Sci. 2021;11(4):1713.
6.    Osanloo M, Noori F, Varaa N, Tavassoli A, Goodarzi A, Moghaddam MT, et al. The wound healing effect of polycaprolactone-chitosan scaffold coated with a gel containing Zataria multiflora Boiss. volatile oil nanoemulsions. BMC Complement Med Ther. 2024;24(1):56.
7.    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 May 6;26(9):2723. doi: 10.3390/molecules26092723. PMID: 34066411; PMCID: PMC8125478.
8.    Kavoosi G, Teixeira da Silva JA, Saharkhiz MJ. Inhibitory effects of Zataria multiflora essential oil and its main components on nitric oxide and hydrogen peroxide production in lipopolysaccharide-stimulated macrophages. J Pharm Pharmacol. 2012 Oct;64(10):1491-500. doi: 10.1111/j.2042-7158.2012.01510.x. Epub 2012 Apr 5. PMID: 22943180.
9.    Weinstein MP, Lewis JS 2nd. The Clinical and Laboratory Standards Institute Subcommittee on Antimicrobial Susceptibility Testing: Background, Organization, Functions, and Processes. J Clin Microbiol. 2020 Feb 24;58(3):e01864-19. doi: 10.1128/JCM.01864-19. PMID: 31915289; PMCID: PMC7041576.
10.    Wikler MA, Cockerill FR, Craig WA, Dudley MN, Eliopoulos GM, Hecht DW et al. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically ; approved standard. 7th ed. Pennsylvania (USA): Wayne; 2006. p. 9-18. 
11.    Alizade Naini M, Mehrvarzi S, Zargari-Samadnejadi A, Tanideh N, Ghorbani M, Dehghanian A, et al. The Antioxidant and Anti-Inflammatory Effects of Quercus brantii Extract on TNBS-Induced Ulcerative Colitis in Rats. Evid Based Complement Alternat Med. 2021 Jan 7;2021:3075973. doi: 10.1155/2021/3075973. PMID: 33505492; PMCID: PMC7808820.
12.    Gouma E, Simos Y, Verginadis I, Lykoudis E, Evangelou A, Karkabounas S. A simple procedure for estimation of total body surface area and determination of a new value of Meeh's constant in rats. Lab Anim. 2012 Jan;46(1):40-5. doi: 10.1258/la.2011.011021. Epub 2011 Oct 18. PMID: 22008848.
13.    Gilpin DA. Calculation of a new Meeh constant and experimental determination of burn size. Burns. 1996 Dec;22(8):607-11. doi: 10.1016/s0305-4179(96)00064-2. PMID: 8982538.
14.    Li K, Diao Y, Zhang H, Wang S, Zhang Z, Yu B, et al. Tannin extracts from immature fruits of Terminalia chebula Fructus Retz. promote cutaneous wound healing in rats. BMC Complement Altern Med. 2011 Oct 7;11:86. doi: 10.1186/1472-6882-11-86. PMID: 21982053; PMCID: PMC3198757.
15.    Ashkani-Esfahani S, Imanieh MH, Khoshneviszadeh M, Meshksar A, Noorafshan A, Geramizadeh B, et al. The healing effect of arnebia euchroma in second degree burn wounds in rat as an animal model. Iran Red Crescent Med J. 2012 Feb;14(2):70-4. Epub 2012 Feb 1. PMID: 22737558; PMCID: PMC3372044.
16.    Jacobsen F, Fisahn C, Sorkin M, Thiele I, Hirsch T, Stricker I, et al. Efficacy of topically delivered moxifloxacin against wound infection by Pseudomonas aeruginosa and methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother. 2011 May;55(5):2325-34. doi: 10.1128/AAC.01071-10. Epub 2011 Feb 22. PMID: 21343458; PMCID: PMC3088190.
17.    Yates CC, Whaley D, Babu R, Zhang J, Krishna P, Beckman E, et al. The effect of multifunctional polymer-based gels on wound healing in full thickness bacteria-contaminated mouse skin wound models. Biomaterials. 2007 Sep;28(27):3977-86. doi: 10.1016/j.biomaterials.2007.05.008. Epub 2007 May 24. PMID: 17561250; PMCID: PMC2034502.
18.    Ridin RA. Phenotypic Discrimination of Antibiotic Resistance Among P. Aeruginosa Collected from Burn Sample. University of Thi-Qar Journal Of Medicine. 2023;26(2):693-9.
19.    Ardekani NT, Khorram M, Zomorodian K, Yazdanpanah S, Veisi H, Veisi H. Evaluation of electrospun poly (vinyl alcohol)-based nanofiber mats incorporated with Zataria multiflora essential oil as potential wound dressing. Int J Biol Macromol. 2019 Mar 15;125:743-750. doi: 10.1016/j.ijbiomac.2018.12.085. Epub 2018 Dec 10. PMID: 30543881.
20.    Zomorodian K, Saharkhiz MJ, Rahimi MJ, Bandegi A, Shekarkhar G, Bandegani A, et al. Chemical composition and antimicrobial activities of the essential oils from three ecotypes of Zataria multiflora. Pharmacogn Mag. 2011 Jan;7(25):53-9. doi: 10.4103/0973-1296.75902. PMID: 21472080; PMCID: PMC3065158.
21.    Reinke JM, Sorg H. Wound repair and regeneration. Eur Surg Res. 2012;49(1):35-43. doi: 10.1159/000339613. Epub 2012 Jul 11. PMID: 22797712.
22.    Farahpour MR, Sheikh S, Kafshdooz E, Sonboli A. Accelerative effect of topical Zataria multiflora essential oil against infected wound model by modulating inflammation, angiogenesis, and collagen biosynthesis. Pharm Biol. 2021 Dec;59(1):1-10. doi: 10.1080/13880209.2020.1861029. PMID: 33378625; PMCID: PMC7782911.
23.    Stupin V, Manturova N, Silina E, Litvitskiy P, Vasin V, Artyushkova E, et al, Gladchenko M, Aliev S. The Effect of Inflammation on the Healing Process of Acute Skin Wounds Under the Treatment of Wounds with Injections in Rats. J Exp Pharmacol. 2020 Oct 30;12:409-422. doi: 10.2147/JEP.S275791. PMID: 33154679; PMCID: PMC7608486.
24.    Costa MF, Durço AO, Rabelo TK, Barreto RSS, Guimarães AG. Effects of Carvacrol, Thymol and essential oils containing such monoterpenes on wound healing: a systematic review. J Pharm Pharmacol. 2019 Feb;71(2):141-155. doi: 10.1111/jphp.13054. Epub 2018 Dec 7. PMID: 30537169.
25.    Sousa LGV, Castro J, Cavaleiro C, Salgueiro L, Tomás M, Palmeira-Oliveira R, Martinez-Oliveira J, Cerca N. Synergistic effects of carvacrol, α-terpinene, γ-terpinene, ρ-cymene and linalool against Gardnerella species. Sci Rep. 2022 Mar 15;12(1):4417. doi: 10.1038/s41598-022-08217-w. PMID: 35292704; PMCID: PMC8924259.
26.    Shokri H, Asadi F, Bahonar AR, Khosravi AR. The Role of Zataria multiflora Essence (Iranian herb) on Innate Immunity of Animal Model. Iran J Immunol. 2006 Dec;3(4):164-8. PMID: 18685176.
27.    Vassiliou E, Awoleye O, Davis A, Mishra S. Anti-Inflammatory and Antimicrobial Properties of Thyme Oil and Its Main Constituents. Int J Mol Sci. 2023 Apr 8;24(8):6936. doi: 10.3390/ijms24086936. PMID: 37108100; PMCID: PMC10138399.
28.    Marchese A, Arciola CR, Barbieri R, Silva AS, Nabavi SF, Tsetegho Sokeng AJ, Izadi M, Jafari NJ, Suntar I, Daglia M, Nabavi SM. Update on Monoterpenes as Antimicrobial Agents: A Particular Focus on p-Cymene. Materials (Basel). 2017 Aug 15;10(8):947. doi: 10.3390/ma10080947. PMID: 28809799; PMCID: PMC5578313.
29.    Günal MY, Okçu Heper A, Zaloğlu N. The effects of topical carvacrol application on wound healing process in male rats. Pharmacog J. 2014.
30.    Vogel HG. Correlation between tensile strength and collagen content in rat skin. Effect of age and cortisol treatment. Connect Tissue Res. 1974;2(3):177-82. doi: 10.3109/03008207409152242. PMID: 4279799.
31.    Khezri K, Farahpour MR, Rad SM. Efficacy of Mentha pulegium essential oil encapsulated into nanostructured lipid carriers as an in vitro antibacterial and infected wound healing agent. Colloids Surf A: Physicochem Eng Asp. 2020;589:124414.
32.    Nair RP, Joseph J, Harikrishnan VS, Krishnan VK, Krishnan L. Contribution of fibroblasts to the mechanical stability of in vitro engineered dermal-like tissue through extracellular matrix deposition. Biores Open Access. 2014 Oct 1;3(5):217-25. doi: 10.1089/biores.2014.0023. PMID: 25371858; PMCID: PMC4215331.
33.    Cho Lee AR, Leem H, Lee J, Park KC. Reversal of silver sulfadiazine-impaired wound healing by epidermal growth factor. Biomaterials. 2005 Aug;26(22):4670-6. doi: 10.1016/j.biomaterials.2004.11.041. Epub 2005 Jan 13. PMID: 15722137.
34.    Rosen J, Landriscina A, Kutner A, Adler BL, Krausz AE, Nosanchuk JD, Friedman AJ. Silver sulfadiazine retards wound healing in mice via alterations in cytokine expression. J Invest Dermatol. 2015 May;135(5):1459-1462. doi: 10.1038/jid.2015.21. Epub 2015 Jan 27. PMID: 25625423.
35.    Muller MJ, Hollyoak MA, Moaveni Z, Brown TL, Herndon DN, Heggers JP. Retardation of wound healing by silver sulfadiazine is reversed by Aloe vera and nystatin. Burns. 2003 Dec;29(8):834-6. doi: 10.1016/s0305-4179(03)00198-0. PMID: 14636760.