Correlation between Major Bioactive Compounds in Essential Oils from Wild and Cultivated Moroccan Plants and their Antibacterial Efficacy against Foodborne Pathogens

Main Article Content

Rachid Amaiach
Sanae Lairini
Mouhcine Fadil
Rabia Bouslamti
Fouad El Akhal
Abdelhakim El Ouali Lalami

Abstract

Foodborne pathogens pose a significant risk due to surface contamination, often from inadequate hygiene or biofilm formation. While chemical disinfectants are commonly used, concerns about harmful by-products have led to the search for natural alternatives. This study aimed to explore the correlation between major compounds and the antibacterial effects of seven Moroccan essential oils (EOs) against common foodborne pathogens. Essential oils were extracted via hydro-distillation and analyzed using gas chromatography-mass spectrometry (GC-MS) and gas chromatography with flame ionization detection (GC-FID). The antibacterial activity was assessed using the disc diffusion method, and multivariate analyses, including principal component analysis (PCA) and hierarchical cluster analysis (HCA), were applied to evaluate correlations between chemical composition and antibacterial efficacy. Forty-five components were identified from the EOs and categorized into 10 chemical classes. Major components included carvacrol (31.93%) in Origanum elongatum, thymol (31.01%) in Thymus vulgaris, linalyl acetate (46.95%) in Citrus aurantium, 1,8-cineole (80.56%) in Eucalyptus globulus, citral (42.69%) in Cymbopogon citratus, borneol (28.10%) in Thymus serpyllum, and camphor (32.25%) in Lavandula stoechas. Strong antibacterial activity was observed in O. elongatum, T. vulgaris, and T. serpyllum, demonstrating bactericidal properties with low minimum inhibitory concentration (MIC) values. In contrast, E. globulus and C. aurantium had higher MIC values. Multivariate analyses revealed that phenols had the most substantial impact on antimicrobial activity, followed by terpenes and alcohols. These findings suggest that Moroccan EOs are promising natural disinfectants for food contact surfaces, reducing the risk of bacterial pathogen transmission.

Article Details

How to Cite
Amaiach, R., Lairini, S., Fadil, M., Bouslamti, R., El Akhal, F., & Lalami, A. E. O. (2024). Correlation between Major Bioactive Compounds in Essential Oils from Wild and Cultivated Moroccan Plants and their Antibacterial Efficacy against Foodborne Pathogens. Tropical Journal of Natural Product Research (TJNPR), 8(10), 8850-8866. https://doi.org/10.26538/tjnpr/v8i10.30
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Articles
Author Biographies

Rachid Amaiach, Laboratory of Materials, Processes, Catalysis, and Environment, Higher School of Technology, University Sidi Mohamed Ben Abdellah, Post office Box 2427 Fez, Morocco

Higher Institute of Nursing Professions and Health Techniques of Fez, Regional Health Directorate, El Ghassani Hospital, 30000 Fez, Morocco

Abdelhakim El Ouali Lalami, Laboratory of Materials, Processes, Catalysis, and Environment, Higher School of Technology, University Sidi Mohamed Ben Abdellah, Post office Box 2427 Fez, Morocco

Higher Institute of Nursing Professions and Health Techniques of Fez, Regional Health Directorate, El Ghassani Hospital, 30000 Fez, Morocco

References

World health organization. WHO’s first ever global estimates of foodborne diseases find children under 5 account for almost one third of deaths. Saudi Med J. 2016; 37(1):109-110. http://www.who.int/mediacentre/news/releases/2015/foodborne-disease-estimates/en/.

Amaiach R, Lairini S, Fadil M, Benboubker M, Bouslamti R, El Amrani, S, El Ouali Lalami, A. Microbiological profile and hygienic quality of foodstuffs marketed in collective catering in central Morocco. Int J Food Sci. 2023; 2023:1–13. https://doi.org/10.1155/2023/2820506.

Simões M, Simões LC, Vieira MJ. A Review of current and emergent biofilm control strategies. LWT - Food Sci Technol. 2010; 43(4):573–583 https://doi.org/10.1016/j.lwt.2009.12.008.

Sharma S, Jaiswal S, Duffy B, Jaiswal AK. Advances in emerging technologies for the decontamination of the food contact surfaces. Food Res Int. 2022; 151, 110865. https://doi.org/10.1016/j.foodres.2021.110865.

Santos MIS, Marques C, Mota J, Pedroso L, Lima A. Applications of essential oils as antibacterial agents in minimally processed fruits and vegetables—A review. Microorganisms. 2022; 10(4), 760. https://doi.org/10.3390/microorganisms10040760.

Collins DB, Farmer DK. Unintended consequences of air cleaning chemistry. Environ Sci Technol. 2021; 55(18):12172–12179. https://doi.org/10.1021/acs.est.1c02582.

Cui H, Zhang C, Li C, Lin L. Antimicrobial mechanism of clove oil on Listeria monocytogenes. Food Control. 2018; 94:140–146. https://doi.org/10.1016/j.foodcont.2018.07.007.

Amiri A, Mottaghipisheh J, Jamshidi-Kia F, Saeidi K, Vitalini S, Iriti M. Antimicorbial potency of major functional foods’ essential oils in liquid and vapor phases: A short review. Appl Sci. 2020; 10(22), 8103. https://doi.org/10.3390/app10228103.

Rossi C, Chaves-López C, Serio A, Casaccia M, Maggio F,Paparella A. Effectiveness and mechanisms of essential oils for biofilm control on food-contact surfaces: An updated review. Crit Rev Food Sci Nutr. 2022; 62(8):2172–2191. https://doi.org/10.1080/10408398.2020.1851169.

Soni KA, Oladunjoye A, Nannapaneni R, Schilling MW, Silva JL, Mikel B, Bailey RH. Inhibition and inactivation of Salmonella typhimurium biofilms from polystyrene and stainless steel surfaces by essential oils and phenolic constituent carvacrol. J Food Prot. 2013; 76(2):205–212. https://doi.org/10.4315/0362-028X.JFP-12-196.

Lu WC, Huang DW, Wang CCR,Yeh CH,Tsai JC, Huang YT, Li PH. Preparation, characterization, and antimicrobial activity of nanoemulsions incorporating citral essential oil. J Food Drug Anal. 2018; 26(1):82–89. https://doi.org/10.1016/j.jfda.2016.12.018.

El Harsal A, Ibn Mansour A, Skali Senhaji N, Ouardy Khay E, Bouhdid S, Amajoud N, Farah A, Belmehdi O, Abrini J. Influence of extraction time on the yield, chemical composition, and antibacterial activity of the essential oil from Origanum elongatum (E. & M.) harvested at northern Morocco. J Essent Oil Bear Plants. 2018; 21(6):1460–1474. https://doi.org/10.1080/0972060X.2019.1572545.

Radi M, Eddardar Z,Drioiche A, Remok F, Hosen MdE, Zibouh K, Ed-Damsyry B, Bouatkiout A, Amine S, Touijer H, Salamatullah AM, Bourhia M, Ibenmoussa S, Zair T. Comparative study of the chemical composition, antioxidant, and antimicrobial activity of the essential oils extracted from Lavandula abrialis and Lavandula stoechas: In vitro and in silico analysis. Front Chem. 2024; 12, 1353385. https://doi.org/10.3389/fchem.2024.1353385.

El Guerrouj B, Taibi M, Elbouzidi A, Bouhassoun S, Loukili EH, Moubchir T, Haddou M, Hammouti Y, Khoulati A, Addi M, Chaabane K, Asehraou A, Bellaouchi R. The effect of altitude on the chemical composition, antioxidant and antimicrobial activities of Eucalyptus globulus Labill. essential oils. Trop J Nat Prod Res. 2023; 7(11):5279-5285. http://www.doi.org/10.26538/tjnpr/v7i11.37.

Bouyahya A, Et-Touys A, Abrini J, Talbaoui A, Fellah H, Bakri Y, Dakka N. Lavandula stoechas essential oil from morocco as novel source of antileishmanial, antibacterial and antioxidant activities. Biocatal Agric Biotechnol. 2017; 12:179–184. https://doi.org/10.1016/j.bcab.2017.10.003.

Benali T, Lemhadri A, Harboul K, Chtibi H, Khabbach A, Jadouali SM, Quesada-Romero L, Louahlia S, Hammani K, Ghaleb A, Lee LH, Bouyahya A, Rusu ME, Akhazzane M. Chemical profiling and biological properties of essential oils of Lavandula stoechas L. collected from three Moroccan sites: In vitro and in silico investigations. Plants. 2023; 12(6), 1413. https://doi.org/10.3390/plants12061413.

El Yaagoubi M, Mechqoq H, El Hamdaoui A, Jrv Mukku V, El Mousadi, A, Msanda F, El Aouad NA. Review on Moroccan thymus species: Traditional uses, essential oils chemical composition and biological effects. J Ethnopharmacol. 2021; 278, 114205. https://doi.org/10.1016/j.jep.2021.114205.

Mouatassem Filali T, Faraj C, Guemmouh R, Fadil M, Rais N, El Asmi H, El-Akhal F, El Fattouhi Y, Darkaoui N, Baghouz A, El Ouali Lalami A. Biotypology of culicidian species in the region of Fez, central Morocco using the statistical analytical methods. Trop J Nat Prod Res. 2024; 8(5):7172-7180. https://doi.org/10.26538/tjnpr/v8i5.19

Babushok VI, Linstrom PJ, Zenkevich IG. Retention indices for frequently reported compounds of plant essential oils. J Phys Chem Ref Data. 2011; 40(4), 043101. https://doi.org/10.1063/1.3653552.

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

Moumni S, Elaissi A, Trabelsi A, Merghni A, Chraief I, Jelassi B, Chemli R, Ferchichi S. Correlation between chemical composition and antibacterial activity of some lamiaceae species essential oils from Tunisia. BMC Complement Med Ther. 2020; 20(1), 103. https://doi.org/10.1186/s12906-020-02888-6.

Bouhdid S, Abrini J, Zhiri A, Espuny MJ, Manresa A. Investigation of functional and morphological changes in Pseudomonas aeruginosa and Staphylococcus aureus cells induced by Origanum compactum essential oil. J Appl Microbiol. 2009; 106(5):1558–1568. https://doi.org/10.1111/j.1365-2672.2008.04124.x.

Basri DF, Luoi CK, Azmi AM, Latip J. Evaluation of the combined effects of stilbenoid from Shorea gibbosa and vancomycin against methicillin-resistant Staphylococcus aureus (MRSA). Pharmaceuticals .2012; 5(9):1032–1043. https://doi.org/10.3390/ph5091032.

Tagnaout I, Zerkani H, Bencheikh N, Amalich S, Bouhrim M, Mothana RA, Alhuzani MR, Bouharroud R, Hano C, Zair T. Chemical composition, antioxidants, antibacterial, and insecticidal activities of Origanum elongatum (Bonnet) Emberger & Maire aerial part essential oil from Morocco. Antibiotics .2023; 12(1), 174. https://doi.org/10.3390/antibiotics12010174.

Oualili H, Nmila R, Chibi F, Lasky M, Mricha A, Rchid H. Chemical composition and antioxidant activity of Origanum elongatum essential oil. Phcog Res. 2019; 11(3), 283. https://doi.org/10.4103/pr.pr_157_18.

Ramzi H, Ismaili MR, Aberchane M, Zaanoun S. Chemical characterization and acaricidal activity of Thymus satureioides C. B. and Origanum elongatum E. & M. (Lamiaceae) essential oils against varroa destructor Anderson & Trueman (Acari: Varroidae). Ind Crops Prod. 2017, 108: 201–207. https://doi.org/10.1016/j.indcrop.2017.06.031.

Bakha M, El Mtili N, Machon N, Aboukhalid K, Amchra FZ, Khiraoui A, Gibernau M, Tomi F, Al Faiz C. Intraspecific chemical variability of the essential oils of Moroccan endemic Origanum elongatum L. (Lamiaceae) from its whole natural habitats. Arabian J Chem. 2020; 13(1):3070–3081. https://doi.org/10.1016/j.arabjc.2018.08.015.

Abdelaali B, El Menyiy N, El Omari N, Benali T, Guaouguaou FE, Salhi N, Naceiri Mrabti H, Bouyahya A. Phytochemistry, Toxicology, and Pharmacological Properties of Origanum elongatum. J Evid Based Complementary Altern Med.2021; 2021:1–12. https://doi.org/10.1155/2021/6658593.

Imelouane B, Amhamdi H, Wathelet JP, Ankit M, Khedid K, Bachiri AE. Chemical Composition and Antimicrobial Activity of Essential Oil of Thyme (Thymus vulgaris) from Eastern Morocco. Int J Agric Biol. 2009; 11(2).

Lemrhari A, Zouhair R, Elidrissi M, Amechrouq A, Elhourri M. Chemical composition and differentiation of essential oils of Morocco’s different varieties of thyme. Global J Pure Appl Sci. 2015; 3(2):24–34.

Sadiki M, Elabed A, Elaabedy A, Elabed S, Farah A, Iraqui M, Koraichi SI. Characterization and antibacterial activity of the essential oil from Thymus vulgaris cultivated in Morocco (Taounate) against ten bacteria. World J Pharm Res.2015; 4(05).

Hattabi LE, Talbaoui A, Amzazi S, Bakri Y, Harhar H, Costa J, Desjobert JM, Tabyaoui M. Chemical composition and antibacterial activity of three essential oils from south of Morocco. (Thymus satureoides, Thymus vulgaris and Chamaelum nobilis). J Mater Environ Sci. 2016b; 7(9):3110–3117.

Jamali CA, El Bouzidi L, Bekkouche K, Lahcen H, Markouk M, Wohlmuth H, Leac, D, Abbad A. Chemical composition and antioxidant and anticandidal activities of essential oils from different wild Moroccan Thymus Species. Chem Biodivers. 2012; 9(6):1188–1197. https://doi.org/10.1002/cbdv.201200041.

Cherrat L, Espina L, Bakkali M, Pagán R, Laglaoui A. Chemical Composition, Antioxidant and Antimicrobial Properties of Mentha pulegium, Lavandula stoechas and Satureja calamintha Scheele essential oils and an evaluation of their bactericidal effect in combined processes. Innovative Food Sci Emerg Technol. 2014; 22:221–229. https://doi.org/10.1016/j.ifset.2013.12.016.

Mekkaoui M, Bouidida EH, Naceiri Mrabti H, Ouaamr A, Lee LH, Bouyahya A, Cherrah Y, Alaoui K. Investigation of chemical compounds and evaluation of toxicity, antibacterial, and anti-inflammatory activities of three selected essential oils and their mixtures with Moroccan thyme honey. Foods. 2022; 11(19), 3141. https://doi.org/10.3390/foods11193141.

Čmiková N, Galovičová L, Schwarzová M, Vukic MD, Vukovic NL, Kowalczewski PŁ, Bakay L, Kluz MI, Puchalski C, Kačániová M. Chemical composition and biological activities of Eucalyptus globulus essential oil. Plants. 2023; 12(5), 1076. https://doi.org/10.3390/plants12051076.

Merghni A, Noumi E, Hadded O, Dridi N, Panwar H, Ceylan O, Mastouri M, Snoussi M. assessment of the antibiofilm and antiquorum sensing activities of Eucalyptus globulus essential oil and its main component 1,8-Cineole against methicillin-resistant Staphylococcus aureus Strains. Microb Pathog. 2018; 118:74–80. https://doi.org/10.1016/j.micpath.2018.03.006.

Bassolé IHN, Lamien-Meda A, Bayala B, Obame LC, Ilboudo AJ, Franz C, Novak J, Nebié RC, Dicko, MH. Chemical composition and antimicrobial activity of Cymbopogon citratus and Cymbopogon giganteus essential oils alone and in combination. Phytomedicine. 2011; 18(12):1070–1074. https://doi.org/10.1016/j.phymed.2011.05.009.

Fouad R, Bousta D, Lalami AEO, Chahdi FO, Amri I, Jamoussi B, Greche H. Chemical composition and herbicidal effects of essential oils of Cymbopogon citratus (DC) Stapf, Eucalyptus cladocalyx, Origanum vulgare L and Artemisia absinthium L. cultivated in Morocco. J Essent Oil Bear Plants. 2015; 18(1):112–123. https://doi.org/10.1080/0972060X.2014.901631.

Tazi A, El Moujahed S, Jaouad N, Saghrouchni H, Al-Ashkar I, Liu L, Errachidi F. Exploring the Bioactive Potential of Moroccan Lemongrass (Cymbopogon citratus): Investigations on molecular weight distribution, antioxidant andantimicrobial potentials. Molecules. 2024; 29(17), 3982; https://doi.org/10.3390/molecules29173982

Ainane T. Chemical characterizations of the aromatic compositions of two citrus species: Citrus aurantium and Citrus reticulata. MOJDDT. 2018; 2 (3). https://doi.org/10.15406/mojddt.2018.02.00032.

Gniewosz M, Kraśniewska K, Kosakowska O, Pobiega K,Wolska I. Chemical compounds and antimicrobial activity of petitgrain (Citrus aurantium L. var. Amara) essential oil. herba Pol. 2017; 63(4):18–25. https://doi.org/10.1515/hepo-2017-0021.

Moussaoui N. Antibacterial and antiviral activities of essential oils of northern Moroccan plants. BBJ. 2013; 3(3):318–331. https://doi.org/10.9734/BBJ/2013/3596.

Kachur K, Suntres Z. The antibacterial properties of phenolic isomers, carvacrol and thymol. Crit Rev

Food Sci Nutr. 2020; 60(18):3042–3053. https://doi.org/10.1080/10408398.2019.1675585.

Drioiche A, Zahra Radi F, Ailli A, Bouzoubaa A, Boutakiout A, Mekdad S, Al Kamaly O, Saleh A, Maouloua M, Bousta D, Sahpaz S, El Makhoukhi F, Zair T. Correlation between the chemical composition and the antimicrobial properties of seven samples of essential oils of endemic thymes in Morocco against multi-resistant bacteria and pathogenic fungi. SPJ. 2022; 30(8), 1200–1214. https://doi.org/10.1016/j.jsps.2022.06.022.

Zantar S, Garrouj D, Pagán R, Chabi M, Laglaoui A, Bakkali M, Zerrouk M. Effect of Harvest Time on Yield, Chemical Composition, Antimicrobial and Antioxidant Activities of Thymus vulgaris and Mentha pulegium Essential Oils. EJMP. 2015; 8(2):69–77. https://doi.org/10.9734/EJMP/2015/17513.

Amarti F, Satrani B, Ghanmi M, Farah A, Aafi A, Aarab L, Ajjouri ME, Chaouch A. Composition chimique et activité antimicrobienne des huiles essentielles de Thymus algeriensis Boiss. & Reut. et Thymus ciliatus (Desf.) Benth. du Maroc. Biotechnol Agron Soc Environ. 2010.

Alaoui Jamali C, Kasrati A, Fadli M, Hassani L, Leach D, Abbad A. Synergistic effects of three Moroccan thyme essential oils with antibiotic cefixime. Phytothérapie 2017. https://doi.org/10.1007/s10298-017-1107-2.

Drioiche A, Baammi S, Zibouh K, Al Kamaly O, Alnakhli AM, Remok F, Saidi S, Amaiach R, El Makhoukhi F, Elomri A, Zair T. A study of the synergistic effects of essential oils from

Origanum compactum and Origanum elongatum with commercial antibiotics against highly prioritized multidrug-resistant bacteria for the world health organization. metabolites. 2024; 14(4), 210. https://doi.org/10.3390/metabo14040210.

Cho TJ, Park SM, Yu H, Seo GH, Kim HW, Kim SA, Rhee MS. Recent advances in the application of antibacterial complexes using essential oils. Molecules. 2020; 25 (7):1752. https://doi.org/10.3390/molecules25071752.