Binary Synergistic Combinations of Lavender and Fennel Essential Oils with Amoxicillin^{[ # ]}

Abstract

Microbial resistance is an important problem in modern healthcare systems. In addition to drug resistance, the side effects of current antibiotic applications are also known issues. In this present study, binary combinations of amoxicillin with European Pharmacopoeia quality lavender (Lavandula angustifolia) and fennel (Foeniculum vulgare) essential oils were evaluated against human pathogenic microbial strains. The checkerboard method was used to quantify the efficacy of the essential oils in combination with amoxicillin. As an initial result, remarkable in vitro antimicrobial activity was observed at relatively low amoxicillin concentrations using different oil combinations against Staphylococcus aureus ATCC 6538, Enterococcus faecalis ATCC 29212, Bacillus cereus ATCC 14579, Escherichia coli NRRL B-3008, Salmonella typhi (clinical isolate), respectively. Fractional inhibitory concentrations were calculated and interpreted in terms of addition, synergy, antagonism, or indifferent. A synergistic interaction with the combination F. vulgare essential oil and amoxicillin (fractional inhibitory concentration index = 8.05 × 10⁻⁴) was observed against the pathogens E. faecalis and Escherichia coli. Both essential oils together and in combination with amoxicillin showed a synergistic effect with possible future applications.

Key words

Lavandula angustifolia - Foeniculum vulgare - amoxicillin - Lamiaceae - Apiaceae - synergism

^# Dedicated to Professor Dr. Gerhard Franz on the occasion of his 85th birthday.

Publication History

Received: 05 February 2022

Accepted after revision: 03 July 2022

Accepted Manuscript online:
04 July 2022

Article published online:
28 September 2022

• References

• 1 Gulfraz M, Mehmood S, Minhas N, Jabeen N, Kausar R, Jabeen K, Arshad G. Composition and antimicrobial properties of essential oil of Foeniculum vulgare . Afric J Biotechnol 2010; 7: 4364-4368
• 2 Kalleli F, Bettaieb Rebey I, Wannes WA, Boughalleb F, Hammami M, Saidani Tounsi M, Mʼhamdi M. Chemical composition and antioxidant potential of essential oil and methanol extract from Tunisian and French fennel (Foeniculum vulgare Mill.) seeds. J Food Biochem 2019; 43: e12935
• 3 Telci I, Demirtas I, Sahin A. Variation in plant properties and essential oil composition of sweet fennel (Foeniculum vulgare Mill.) fruits during stages of maturity. Ind Crops Prod 2009; 30: 126-130
• 4 Diao WR, Hu QP, Zhang H, Xu JG. Chemical composition, antibacterial activity and mechanism of action of essential oil from seeds of fennel (Foeniculum vulgare Mill.). Food Control 2014; 35: 109-116
• 5 Mimica-Dukić N, Kujundžić S, Soković M, Couladis M. Essential oil composition and antifungal activity of Foeniculum vulgare Mill obtained by different distillation conditions. Phytother Res 2003; 17: 368-371
• 6 Özbek H, Ugras S, Tuncer I, Bayram I, Tuncer I, Öztürk G, Öztürk A. Hepatoprotective effect of Foeniculum vulgare essential oil. Fitoterapia 2003; 74: 317-319
• 7 Kerekes D, Csorba A, Gosztola B, Németh-Zámbori É, Kiss T, Csupor D. Furocoumarin content of fennel–below the safety threshold. Molecules 2019; 24: 2844
• 8 European Medicines Agency (EMA). Committee on Herbal Medicinal Products (HPMC). Assessment Report on Foeniculum vulgare Miller. Evaluation of Medicines for Human Use. Accessed May 21, 2022 at: https://www.ema.europa.eu/en/documents/herbal-report/assessment-report-foeniculum-vulgare-miller_en.pdf
• 9 Leong WH, Lai KS, Lim SHE. Combination therapy involving Lavandula angustifolia and its derivatives in exhibiting antimicrobial properties and combatting antimicrobial resistance: current challenges and future prospects. Processes 2021; 9: 609
• 10 Adaszyńska-Skwirzyńska M, Szczerbińska D. The antimicrobial activity of lavender essential oil (Lavandula angustifolia) and its influence on the production performance of broiler chickens. J Anim Physiol Anim Nutr 2018; 102: 1020-1025
• 11 Niksic H, Kovac-Besovic E, Omeragic E, Muratovic S, Kusturica J, Duric K. Antiproliferative, antimicrobial, and antioxidant activity of Lavandula angustifolia Mill. essential oil. J Health Sci 2017; 7: 35
• 12 López V, Nielsen B, Solas M, Ramírez MJ, Jäger AK. Exploring pharmacological mechanisms of lavender (Lavandula angustifolia) essential oil on central nervous system targets. Front Pharmacol 2017; 8: 280
• 13 European Medicines Agency (EMA). Community herbal monograph on Lavandula angustifolia Miller, aetheroleum. Accessed May 21, 2022 at: https://www.ema.europa.eu/en/documents/herbal-monograph/final-community-herbal-monograph-lavandula-angustifolia-miller-aetheroleum_en.pdf
• 14 Roller S, Ernest N, Buckle J. The antimicrobial activity of high-necrodane and other lavender oils on methicillin-sensitive and-resistant Staphylococcus aureus (MSSA and MRSA). J Altern Complement Med 2009; 15: 275-279
• 15 Rai VK, Sinha P, Yadav KS, Shukla A, Saxena A, Bawankule DU, Yadav NP. Anti-psoriatic effect of Lavandula angustifolia essential oil and its major components linalool and linalyl acetate. J Ethnopharmacol 2020; 261: 113127
• 16 Abdel-Baki AAS, Aboelhadid SM, Sokmen A, Al-Quraishy S, Hassan AO, Kamel AA. Larvicidal and pupicidal activities of Foeniculum vulgare essential oil, trans-anethole and fenchone against house fly Musca domestica and their inhibitory effect on acetylcholinestrase. Entomol Res 2021; 51: 568-577
• 17 El Atki Y, Aouam I, El Kamari F, Taroq A, Nayme K, Timinouni M, Abdellaoui A. Antibacterial activity of cinnamon essential oils and their synergistic potential with antibiotics. J Advan Pharm Technol Res 2019; 10: 63
• 18 Hossain S, Heo H, De Silva BCJ, Wimalasena SHMP, Pathirana HNKS, Heo GJ. Antibacterial activity of essential oil from lavender (Lavandula angustifolia) against pet turtle-borne pathogenic bacteria. Lab Animal Res 2017; 33: 195-201
• 19 Smigielski K, Prusinowska R, Stobiecka A, Kunicka-Styczyñska A, Gruska R. Biological properties and chemical composition of essential oils from flowers and aerial parts of lavender (Lavandula angustifolia). J Essent Oil Bear Plants 2018; 21: 1303-1314
• 20 Jianu C, Lukinich-Gruia AT, Horhat FG. Chemical composition and antimicrobial activity of essential oils of lavender (Lavandula angustifolia) and lavandin (Lavandula x intermedia) grown in Western Romania. Int J Agricult Biol 2013; 15: 772-776
• 21 Tardugno R, Serio A, Pellati F, DʼAmato S, Chaves López C, Bellardi MG, Benvenuti S. Lavandula x intermedia and Lavandula angustifolia essential oils: phytochemical composition and antimicrobial activity against foodborne pathogens. Nat Prod Res 2019; 33: 3330-3335
• 22 Danh LT, Han LN, Triet NDA, Zhao J, Mammucari R, Foster N. Comparison of chemical composition, antioxidant and antimicrobial activity of lavender (Lavandula angustifolia L.) essential oils extracted by supercritical CO₂, hexane and hydrodistillation. Food Bioproc Technol 2013; 6: 3481-3489
• 23 Zengin H, Baysal AH. Antibacterial and antioxidant activity of essential oil terpenes against pathogenic and spoilage-forming bacteria and cell structure-activity relationships evaluated by SEM microscopy. Molecules 2014; 19: 17773-17798
• 24 Herman A, Tambor K, Herman A. Linalool affects the antimicrobial efficacy of essential oils. Curr Microbiol 2016; 72: 165-172
• 25 Beier RC, Byrd 2nd JA, Kubena LF, Hume ME, McReynolds JL, Anderson RC, Nisbet DJ. Evaluation of linalool, a natural antimicrobial and insecticidal essential oil from basil: effects on poultry. Poult Sci 2014; 93: 267-272
• 26 Alviano WS, Mendonça-Filho RR, Alviano DS, Bizzo HR, Souto-Padrón T, Rodrigues ML, Souza MMG. Antimicrobial activity of Croton cajucara Benth linalool-rich essential oil on artificial biofilms and planktonic microorganisms. Oral Microbiol Immunol 2005; 20: 101-105
• 27 Aelenei P, Rimbu CM, Guguianu E, Dimitriu G, Aprotosoaie AC, Brebu M, Miron A. Coriander essential oil and linalool – interactions with antibiotics against Gram-positive and Gram-negative bacteria. Lett App Microbiol 2019; 68: 156-164
• 28 de Rapper S, Viljoen A, van Vuuren S. The in vitro antimicrobial effects of Lavandula angustifolia essential oil in combination with conventional antimicrobial agents. Evid Based Complement Alternat Med 2016; 2016: 2752739
• 29 Anwar F, Ali M, Hussain AI, Simões MT, Figueiredo AC, Barroso JG, Pedro LG. Antioxidant and antimicrobial activities of essential oil and extracts of fennel (Foeniculum vulgare Mill.) seeds from Pakistan. Flavour Fragr J 2009; 24: 170-176
• 30 Miguel MG, Cruz C, Faleiro L. Foeniculum vulgare essential oils: chemical composition, antioxidant and antimicrobial activities. Nat Prod Commun 2010; 5: 319-328
• 31 Roby MHH, Sarhan MA, Selim KAH, Khalel KI. Antioxidant and antimicrobial activities of essential oil and extracts of fennel (Foeniculum vulgare L.) and chamomile (Matricaria chamomilla L.). Ind Crops Prod 2013; 44: 437-445
• 32 Zeng H, Chen X, Liang J. In vitro antifungal activity and mechanism of essential oil from fennel (Foeniculum vulgare L.) on dermatophyte species. J Med Microbiol 2015; 64: 93-103
• 33 Mansour SA, Heikal TM, Refaie AA, Mossa AH. Antihepatotoxic activity of fennel (Foeniculum vulgare Mill.) essential oil against chlorpyrifos-induced liver injury in rats. Glob J Environ Sci Technol 2011; 1: 1-11
• 34 Sharopov F, Valiev A, Satyal P, Gulmurodov I, Yusufi S, Setzer WN, Wink M. Cytotoxicity of the essential oil of fennel (Foeniculum vulgare) from Tajikistan. Foods 2017; 6: 73
• 35 Langeveld WT, Veldhuizen EJA, Burt SA. Synergy between essential oil components and antibiotics: a review. Critic Rev Microbiol 2014; 40: 76-94
• 36 White RL, Burgess DS, Manduru M, Bosso JA. Comparison of three different in vitro methods of detecting synergy: time-kill, checkerboard, and E test. Antimic Agent Chemother 1996; 40: 1914-1918
• 37 Orhan G, Bayram A, Zer Y. Synergy tests by E test and checkerboard methods of antimicrobial combinations against Brucella melitensis . J Clin Microbiol 2005; 43: 140-143
• 38 Chanda S, Rakholiya KD, Rakholiya K. Combination therapy: Synergism between natural plant extracts and antibiotics against infectious diseases. Microbiol Book Series 2011; 1: 520-529
• 39 Bassolé IHN, Juliani HR. Essential oils in combination and their antimicrobial properties. Molecules 2012; 17: 3989-4006
• 40 Kwiatkowski P, Pruss A, Masiuk H, Mnichowska-Polanowska M, Kaczmarek M, Giedrys-Kalemba S, Sienkiewicz M. The effect of fennel essential oil and trans-anethole on antibacterial activity of mupirocin against Staphylococcus aureus isolated from asymptomatic carriers. Postepy Dermatol Alergol 2019; 36: 308-314
• 41 Demirci F, Terali K, Karadağ AE, Biltekin SN, Sakallı EA, Koşar M, Demirci B, Baser KHC. In vitro and in silico evaluation of ACE2 and LOX inhibitory activity of Origanum essential oils and Carvacrol. Planta Med 2022;
• 42 Clinical Laboratory and Science Institute (CLSI). Methods for Dilution antimicrobial Susceptibility Tests for Bacteria that grow aerobically. Approved Standard M7-A6, National Committee for Clinical Laboratory Standards, 7th edition. Wayne, Pa, USA: Clinical Laboratory and Science Institute; 2006
• 43 Bonapace CR, Bosso JA, Friedrich L, White RL. Comparison of methods of interpretation of checkerboard synergy testing. Diagn Microbiol Infect Dis 2002; 44: 363-366
• 44 Babushok VI, Linstrom PJ, Zenkevich IG. Retention indices for frequently reported compounds of plant essential oils. J Phys Chem Ref Data 2011; 40: 1-47
• 45 Abdelwahed A, Hayder N, Kilani S, Mahmoud A, Chibani J, Hammami M, Chekir-Ghedira L, Ghedira K. Chemical composition and antimicrobial activity of essential oils from Tunisian Pituranthos tortuosus (Coss.) Maire. Flavour Fragr J 2006; 21: 129-133
• 46 Viljoen AM, Kamatou GPP, Coovadia ZH, Ozek T, Baser KHC. Rare sesquiterpenes from South African Pteronia species. South Afr J Bot 2011; 76: 146-152