Combined antibacterial effect of Origanum compactum and Mentha piperita (Lamiaceae) essential oils against ATCC Escherichia coli and Staphylococcus aureus

, , , , , , , , ,


Research Articles | Published:

Print ISSN : 0970-4078.
Online ISSN : 2229-4473.
Website:www.vegetosindia.org
Pub Email: contact@vegetosindia.org
Doi: 10.1007/s42535-021-00276-0
First Page: 74
Last Page: 82
Views: 1988


Keywords: Antimicrobial activity, Essential oil, Mentha piperita L., Origanum compactum L., Synergistic effect


Abstract


With the increasing concerns about the safety of chemical synthetic substances being added to food products, companies are beginning to search for natural sources of antimicrobials. Because essential oils were proven to have antimicrobial properties, they can be used as food preservatives. The mixture of essential oils may have a more potent antimicrobial profile compared to any single essential oil. Hence, the purpose of this work was to determine the chemical composition and inhibitory effects of Origanum compactum L. and Mentha piperita L. (Lamiaceae) essential oils alone or in combination against Staphylococcus aureus ATCC 29,213 and Escherichia coli ATCC 25,922. It is the first time reporting a combination of these two essential oils to control foodborne pathogens type Escherichia coli and Staphylococcus aureus. The major constituents of O. compactum essential oil were determined as carvacrol, thymol, p-cymene, and α-terpinene. Regarding M. piperita essential oil, menthofuran, menthol, methyl acetate, 1,8 cineole, and β-pinene were the major compounds. The mixture of essential oils presented a strong synergistic effect against E. coli, decreasing the minimum inhibitory concentration (MIC) of O. compactum from 0.0625% to 0.015625% (v/v) and the MIC of M. piperita from 1% to 0.125% (v/v). It was concluded that a mixture of essential oils provides a better antimicrobial effect against tested bacteria than that of the essential oils alone.


Antimicrobial activity, Essential oil, 
                        Mentha piperita L., 
                        Origanum compactum L., Synergistic effect


*Get Access

(*Only SPR Members can get full access. Click Here to Apply and get access)

Advertisement

References


Aboukhalid K, Lamiri A, Agacka-Mołdoch M, Doroszewska T, Douaik A, Bakha M, Casanova J, Tomi F, Machon N, Faiz CA (2016) Chemical polymorphism of Origanum compactum grown in all natural habitats in Morocco. Chem Biodivers 13:1126–1139. https://doi.org/10.1002/cbdv.201500511


Adrar N, Oukil N, Bedjou F (2016) Antioxidant and antibacterial activities of Thymus numidicus and Salvia officinalis essential oils alone or in combination. Ind Crops Prod 88:112–119. https://doi.org/10.1016/j.indcrop.2015.12.007


Ahmad A, Khan A, Samber N, Manzoor N (2014) Antimicrobial activity of Mentha piperita essential oil in combination with silver ions. Synergy 1:92–98. https://doi.org/10.1016/j.synres.2014.11.001


Amiri H (2012) Essential oils composition and antioxidant properties of three Thymus species. Evid Based Complement Alternat Med 2012:1–8. https://doi.org/10.1155/2012/728065


Andrade-Ochoa S, Nevárez-Moorillón GV, Sánchez-Torres LE, Villanueva-García M, Sánchez-Ramírez BE, Rodríguez-Valdez LM, Rivera-Chavira BE (2015) Quantitative structure-activity relationship of molecules constituent of different essential oils with antimycobacterial activity against Mycobacterium tuberculosis and Mycobacterium bovis. BMC Complement Altern Med 15:332. https://doi.org/10.1186/s12906-015-0858-2


Ayari S, Shankar S, Follett P, Hossain F, Lacroix M (2020) Potential synergistic antimicrobial efficiency of binary combinations of essential oils against Bacillus cereus and Paenibacillus amylolyticus-part A. Microb Pathog 141:104008. https://doi.org/10.1016/j.micpath.2020.104008


Babili FE, Bouajila J, Souchard JP, Bertrand C, Bellvert F, Fouraste I, Moulis C, Valentin A (2011) Oregano: chemical analysis and evaluation of its antimalarial, antioxidant, and cytotoxic activities. J Food Sci 76:C512–C518. https://doi.org/10.1111/j.1750-3841.2011.02109.x


Bag A, Chattopadhyay RR (2015) Evaluation of synergistic antibacterial and antioxidant efficacy of essential oils of spices and herbs in combination. PLoS ONE 10:e0131321. https://doi.org/10.1371/journal.pone.0131321


Bakhy K, Benlhabib O, Bighelli A, Casanova J, Tomi F, Faiz CA (2014) Yield and chemical variability of the essential oil isolated from aerial parts of wild Origanum compactum Benth. From Moroc West Rif 4:9–17


Basri DF, Luoi CK, Azmi AM, Latip J (2012) Evaluation of the combined effects of stilbenoid from Shorea gibbosa and vancomycin against methicillin-resistant Staphylococcus aureus (MRSA). Pharmaceuticals 5:1032–1043. https://doi.org/10.3390/ph5091032


Bassolé IHN, Lamien-Meda A, Bayala B, Tirogo S, Franz C, Novak J, Nebié RC, Dicko MH (2010) Composition and antimicrobial activities of Lippia multiflora Moldenke, Mentha piperita L. and Ocimum basilicum L. essential oils and their major monoterpene alcohols alone and in Combination. Molecules 15:7825–7839. https://doi.org/10.3390/molecules15117825


Benabdallah A, Boumendjel M, Aissi O, Rahmoune C, Boussaid M, Messaoud C (2018) Chemical composition, antioxidant activity and acetylcholinesterase inhibitory of wild Mentha species from northeastern Algeria. South Afr J Bot 116:131–139. https://doi.org/10.1016/j.sajb.2018.03.002


Bouchra C, Achouri M, Idrissi Hassani LM, Hmamouchi M (2003) Chemical composition and antifungal activity of essential oils of seven Moroccan Labiatae against Botrytis cinerea Pers: Fr. J Ethnopharmacol 89:165–169. https://doi.org/10.1016/S0378-8741(03)00275-7


Bouhdid S, Skali SN, Idaomar M, Zhiri A, Baudoux D, Amensour M, Abrini J (2008) Antibacterial and antioxidant activities of Origanum compactum essential oil. Afr J Biotech 7(10):1563–1570


Bouyahya A, Dakka N, Talbaoui A, Et-Touys A, El-Boury H, Abrini J, Bakri Y (2017) Correlation between phenological changes, chemical composition and biological activities of the essential oil from Moroccan endemic oregano (Origanum compactum Benth). Ind Crops Prod 108:729–737. https://doi.org/10.1016/j.indcrop.2017.07.033


Bouyahya A, Dakka N, Lagrouh F, Abrini J, Bakri Y (2019) Anti-dermatophytes activity of Origanum compactum essential oil at three developmental stages. Phytothérapie 17:201–205. https://doi.org/10.3166/phyto-2018-0063


Bouyahya A, Belmehdi O, Benjouad A, Ameziane El Hassani R, Amzazi S, Dakka N, Bakri Y (2020) Pharmacological properties and mechanism insights of Moroccan anticancer medicinal plants: what are the next steps? Ind Crops Prod 147:112198. https://doi.org/10.1016/j.indcrop.2020.112198


Calderón-Oliver M, Escalona-Buendía HB, Medina-Campos ON, Pedraza-Chaverri J, Pedroza-Islas R, Ponce-Alquicira E (2016) Optimization of the antioxidant and antimicrobial response of the combined effect of nisin and avocado byproducts. LWT Food Sci Technol 65:46–52. https://doi.org/10.1016/j.lwt.2015.07.048


Chauhan AK, Kang SC (2014) Thymol disrupts the membrane integrity of Salmonella typhimurium in vitro and recovers infected macrophages from oxidative stress in an ex vivo model. Res Microbiol 165:559–565. https://doi.org/10.1016/j.resmic.2014.07.001


Cho Y, Kim H, Beuchat LR, Ryu J-H (2020) Synergistic activities of gaseous oregano and thyme thymol essential oils against Listeria monocytogenes on surfaces of a laboratory medium and radish sprouts. Food Microbiol 86:103357. https://doi.org/10.1016/j.fm.2019.103357


Clemente I, Aznar M, Silva F, Nerín C (2016) Antimicrobial properties and mode of action of mustard and cinnamon essential oils and their combination against foodborne bacteria. Innov Food Sci Emerg Technol 36:26–33. https://doi.org/10.1016/j.ifset.2016.05.013


de Azeredo GA, Stamford TLM, Nunes PC, Gomes Neto NJ, de Oliveira MEG, de Souza EL (2011) Combined application of essential oils from Origanum vulgare L. and Rosmarinus officinalis L. to inhibit bacteria and autochthonous microflora associated with minimally processed vegetables. Food Res Int 44:1541–1548. https://doi.org/10.1016/j.foodres.2011.04.012


de Sousa Guedes JP, da Costa Medeiros JA, de Souza e Silva RS, de Sousa JMB, da Conceição ML, de Souza EL (2016) The efficacy of Mentha arvensis L. and M. piperita L. essential oils in reducing pathogenic bacteria and maintaining quality characteristics in cashew, guava, mango, and pineapple juices. Int J Food Microbiol 238:183–192. https://doi.org/10.1016/j.ijfoodmicro.2016.09.005


Desam NR, Al-Rajab AJ, Sharma M, Mylabathula MM, Gowkanapalli RR, Albratty M (2017) Chemical constituents, in vitro antibacterial and antifungal activity of Mentha Piperita L. (peppermint) essential oils. J King Saud Univ Sci 31(2019):528–533. https://doi.org/10.1016/j.jksus.2017.07.013


El amrani S, El Ouali Lalami A, Ez zoubi Y, Moukhafi K, Bouslamti R, Lairini S (2019) Evaluation of antibacterial and antioxidant effects of cinnamon and clove essential oils from Madagascar. Mater Today Proc 13:762–770. https://doi.org/10.1016/j.matpr.2019.04.038


Ez zoubi Y, Farah A, Zaroual H, El Ouali Lalami A (2020) Antimicrobial activity of Lavandula stoechas phenolic extracts against pathogenic bacteria isolated from hospital in Morocco. Vegetos 33(4):703–711


Fraj A, Jaâfar F, Marti M, Coderch L, Ladhari N (2019) A comparative study of oregano (Origanum vulgare L.) essential oil-based polycaprolactone nanocapsules/microspheres: preparation, physicochemical characterization, and storage stability. Ind Crops Prod 140:111669. https://doi.org/10.1016/j.indcrop.2019.111669


Frezza C, Venditti A, Serafini M, Bianco A (2019) Phytochemistry, chemotaxonomy, ethnopharmacology, and nutraceutics of Lamiaceae. Stud Nat Prod Chem 62:125–178. https://doi.org/10.1016/B978-0-444-64185-4.00004-6


Gallucci MN, Oliva M, Casero C, Dambolena J, Luna A, Zygadlo J, Demo M (2009) Antimicrobial combined action of terpenes against the food-borne microorganisms Escherichia coli, Staphylococcus aureus and Bacillus cereus. Flavour Fragr J 24:348–354. https://doi.org/10.1002/f.1948


Garzoli S, Petralito S, Ovidi E, Turchetti G, Laghezza Masci V, Tiezzi A, Trilli J, Cesa S, Casadei MA, Giacomello P, Paolicelli P (2020) Lavandula intermedia essential oil and hydrolate: evaluation of chemical composition and antibacterial activity before and after formulation in nanoemulsion. Ind Crops Prod 145:112068. https://doi.org/10.1016/j.indcrop.2019.112068


Ghabraie M, Vu KD, Tata L, Salmieri S, Lacroix M (2016) Antimicrobial effect of essential oils in combinations against five bacteria and their effect on sensorial quality of ground meat. LWT Food Sci Technol 66:332–339. https://doi.org/10.1016/j.lwt.2015.10.055


Gutierrez J, Barry-Ryan C, Bourke P (2008) The antimicrobial efficacy of plant essential oil combinations and interactions with food ingredients. Int J Food Microbiol 124:91–97. https://doi.org/10.1016/j.ijfoodmicro.2008.02.028


Hyldgaard M, Mygind T, Meyer RL (2012) Essential oils in food preservation: mode of action, synergies, and interactions with food matrix components. Front Microbiol 3:1–24. https://doi.org/10.3389/fmicb.2012.00012


Jeannot V (2003) Origanum compactum Bentham: composition of the hydrolat aromatic fraction, comparison with the essential oil and its interest in aromatherapy. Int J Aromather 13:90–94. https://doi.org/10.1016/S0962-4562(03)00076-6


Knowles JR, Roller S, Murray DB, Naidu AS (2005) Antimicrobial action of carvacrol at different stages of dual-species biofilm development by Staphylococcus aureus and Salmonella enterica Serovar Typhimurium. Appl Environ Microbiol 71:797–803. https://doi.org/10.1128/AEM.71.2.797-803.2005


Konaté K, Mavoungou J, Lepengué A, Aworet-Samseny RR, Hilou A, Souza A, Dicko MH, M’Batchi B (2012) Antibacterial activity against β-lactamase producing methicillin and ampicillin-resistants Staphylococcus aureus: fractional inhibitory concentration index (FICI) determination. Ann Clin Microbiol Antimicrob 11:18. https://doi.org/10.1186/1476-0711-11-18


Laghmouchi Y, Belmehdi O, Senhaji NS, Abrini J (2018) Chemical composition and antibacterial activity of Origanum compactum Benth. essential oils from different areas at northern Morocco. South Afr J Bot 115:120–125. https://doi.org/10.1016/j.sajb.2018.02.002


Lambert RJW, Skandamis PN, Coote PJ, Nychas G-JE (2001) A study of the minimum inhibitory concentration and mode of action of oregano essential oil, thymol and carvacrol. J Appl Microbiol 91:453–462. https://doi.org/10.1046/j.1365-2672.2001.01428.x


Lamiri A, Lhaloui S, Benjilali B, Berrada M (2001) Insecticidal effects of essential oils against Hessian ¯y, Mayetiola destructor (Say). Field Crops Res 71:9–15


Li G-X, Liu Z-Q (2009) Unusual antioxidant behavior of α- and γ-terpinene in protecting methyl linoleate, DNA, and erythrocyte. J Agric Food Chem 57:3943–3948. https://doi.org/10.1021/jf803358g


Liang X-X, Kong L-X, Fei W-B, He M (2018) Chemical constituents and antibacterial activities of Aspidistra typica. Chin J Nat Med 16:465–470. https://doi.org/10.1016/S1875-5364(18)30080-3


Machiani MA, Javanmard A, Morshedloo MR, Maggi F (2018) Evaluation of yield, essential oil content and compositions of peppermint (Mentha piperita L.) intercropped with faba bean (Vicia faba L.). J Clean Prod 171:529–537. https://doi.org/10.1016/j.jclepro.2017.10.062


Messaoudi Moussii I, Nayme K, Timinouni M, Jamaleddine J, Filali H, Hakkou F (2020) Synergistic antibacterial effects of Moroccan Artemisia herba alba, Lavandula angustifolia and Rosmarinus officinalis essential oils. Synergy 10:100057. https://doi.org/10.1016/j.synres.2019.100057


Mezzoug N, Elhadri A, Dallouh A, Amkiss S, Skali NS, Abrini J, Zhiri A, Baudoux D, Diallo B, El Jaziri M, Idaomar M (2007) Investigation of the mutagenic and antimutagenic effects of Origanum compactum essential oil and some of its constituents. Mutat Res Toxicol Environ Mutagen 629:100–110. https://doi.org/10.1016/j.mrgentox.2007.01.011


Milevskaya VV, Prasad S, Temerdashev ZA (2019) Extraction and chromatographic determination of phenolic compounds from medicinal herbs in the Lamiaceae and Hypericaceae families: a review. Microchem J 145:1036–1049. https://doi.org/10.1016/j.microc.2018.11.041


Moussaoui F, Alaoui T (2016) Evaluation of antibacterial activity and synergistic effect between antibiotic and the essential oils of some medicinal plants. Asian Pac J Trop Biomed 6:32–37. https://doi.org/10.1016/j.apjtb.2015.09.024


Ouedrhiri W, Balouiri M, Bouhdid S, Moja S, Chahdi FO, Taleb M, Greche H (2016) Mixture design of Origanum compactum, Origanum majorana and Thymus serpyllum essential oils: optimization of their antibacterial effect. Ind Crops Prod 89:1–9. https://doi.org/10.1016/j.indcrop.2016.04.049


Ouedrhiri W, Mounyr B, Harki EH, Moja S, Greche H (2017) Synergistic antimicrobial activity of two binary combinations of marjoram, lavender, and wild thyme essential oils. Int J Food Prop 20:3149–3158. https://doi.org/10.1080/10942912.2017.1280504


Ouedrhiri W, Bouhdid S, Balouiri M, Lalami AEO, Moja S, Chahdi FO, Greche H (2015) Chemical composition of Citrus aurantium L. leaves and zest essential oils, their antioxidant, antibacterial single and combined effects. J Chem Pharm Res 7(1):78–84


Oussalah M, Caillet S, Saucier L, Lacroix M (2007) Inhibitory effects of selected plant essential oils on the growth of four pathogenic bacteria: E. coli O157:H7, Salmonella Typhimurium, Staphylococcus aureus and Listeria monocytogenes. Food Control 18:414–420. https://doi.org/10.1016/j.foodcont.2005.11.009


Prakash B, Kujur A, Yadav A, Kumar A, Singh PP, Dubey NK (2018) Nanoencapsulation: an efficient technology to boost the antimicrobial potential of plant essential oils in food system. Food Control 89:1–11. https://doi.org/10.1016/j.foodcont.2018.01.018


Raj A, Menon V, Sharma N (2020) Phytochemical screening, antimicrobial, antioxidant and cytotoxic potential of different extracts of Psidium guajava leaves. Vegetos 33(4):750–758


Sadiki M, Balouiri M, Barkai H, Maataoui H, Ibnsoud S, Elabed S (2014) Synergistic antibacterial effect of Myrtus communis and Thymus vulgaris essential oils fractional inhibitory concentration index. Int J Pharm Pharm Sci 6:5


Sadiki M, Abed SE, Balouiri M, Barkai H, Bergadi FZE, Farricha OE, Koraichi I (2017) Combined effect of essential oils against bacteria associated with deterioration of historical wood. J Mater Environ Sci 8(2):594–602


Satmi FRS, Hossain MA (2016) In vitro antimicrobial potential of crude extracts and chemical compositions of essential oils of leaves of Mentha piperita L. native to the Sultanate of Oman. Pac Sci Rev Nat Sci Eng 18:103–106. https://doi.org/10.1016/j.psra.2016.09.005


Singh R, Shushni MAM, Belkheir A (2015) Antibacterial and antioxidant activities of Mentha piperita L. Arab J Chem 8:322–328. https://doi.org/10.1016/j.arabjc.2011.01.019


Talei G-R, Mohammadi M, Bahmani M, Kopaei M (2017) Synergistic effect of Carum copticum and Mentha piperita essential oils with ciprofloxacin, vancomycin, and gentamicin on Gram-negative and Gram-positive bacteria. Int J Pharm Investig 7:82. https://doi.org/10.4103/jphi.JPHI_12_17


Valero M, Francés E (2006) Synergistic bactericidal effect of carvacrol, cinnamaldehyde or thymol and refrigeration to inhibit Bacillus cereus in carrot broth. Food Microbiol 23:68–73. https://doi.org/10.1016/j.fm.2005.01.016


Van Haute S, Raes K, Van der Meeren P, Sampers I (2016) The effect of cinnamon, oregano and thyme essential oils in marinade on the microbial shelf life of fish and meat products. Food Control 68:30–39. https://doi.org/10.1016/j.foodcont.2016.03.025


Xu J, Zhou F, Ji B-P, Pei R-S, Xu N (2008) The antibacterial mechanism of carvacrol and thymol against Escherichia coli. Lett Appl Microbiol 47:174–179. https://doi.org/10.1111/j.1472-765X.2008.02407.x


Yang S-K, Yap PS-X, Krishnan T, Yusoff K, Chan K-G, Yap W-S, Lai K-S, Lim S-HE (2018) Mode of action: synergistic interaction of peppermint (Mentha piperita L. Carl) essential oil and meropenem against plasmid-mediated resistant E. coli. Rec Nat Prod 12:582–594. https://doi.org/10.25135/rnp.59.17.12.078


Yu X, Liang C, Fang H, Qi X, Li W, Shang Q (2018) Variation of trichome morphology and essential oil composition of seven Mentha species. Biochem Syst Ecol 79:30–36. https://doi.org/10.1016/j.bse.2018.04.016

 


Acknowledgements


We express special gratitude to everyone who contributed to this study.


Author Information


El amrani Soukaina
Materials, Processes, Catalysis and Environment Laboratory, Higher School of Technology of Fez, Sidi Mohamed Ben Abdellah University, Fez, Morocco

Sanae Lairini
Materials, Processes, Catalysis and Environment Laboratory, Higher School of Technology of Fez, Sidi Mohamed Ben Abdellah University, Fez, Morocco


Ez zoubi Yassine
Biotechnology, Environmental Technology and Valorization of Bio-Resources Team, Department of Biology, Faculty of Sciences and Technologies Al-Hoceima, Abdelmalek Essaadi University, Tetouan, Morocco


Evrendilek Gulsun Akdemir
Department of Food Engineering, Faculty of Engineering, Bolu Abant Izzet Baysal University, Bolu, Turkey


Mouhcine Fadil
Physico-chemical laboratory of inorganic and organic materials, Materials Science Center (MSC), Ecole Normale Supérieure, Mohammed V University in rabat, Rabat, Morocco

Hicham Kass
Materials, Processes, Catalysis and Environment Laboratory, Higher School of Technology of Fez, Sidi Mohamed Ben Abdellah University, Fez, Morocco

Rabia Bouslamti
Materials, Processes, Catalysis and Environment Laboratory, Higher School of Technology of Fez, Sidi Mohamed Ben Abdellah University, Fez, Morocco

,
Abdelhakim El Ouali Lalami
Materials, Processes, Catalysis and Environment Laboratory, Higher School of Technology of Fez, Sidi Mohamed Ben Abdellah University, Fez, Morocco
eloualilalami@yahoo.fr
Sanae Lairini
Materials, Processes, Catalysis and Environment Laboratory, Higher School of Technology of Fez, Sidi Mohamed Ben Abdellah University, Fez, Morocco

Ez zoubi Yassine
Biotechnology, Environmental Technology and Valorization of Bio-Resources Team, Department of Biology, Faculty of Sciences and Technologies Al-Hoceima, Abdelmalek Essaadi University, Tetouan, Morocco