Login Register Cart 0
Generic placeholder image

Anti-Infective Agents

Editor-in-Chief

ISSN (Print): 2211-3525
ISSN (Online): 2211-3533

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Research Article

Comparative Phytochemical Composition and Antimicrobial Activity of Citrus Peel Essential Oils and Phenolic Compounds

Author(s): Sara A. Alsakhawy*, Hoda H. Baghdadi, Moustafa A. El‑Shenawy and Lobna S. El‑Hosseiny

Volume 21, Issue 4, 2023

Published on: 13 July, 2023

Article ID: e180423215987 Pages: 12

DOI: 10.2174/2211352521666230418113927

Price: $65

Abstract

Background: Antimicrobial resistance is imposing an alarming public health threat in regard to the irrational use of the currently available antibiotics and the lack of new antimicrobials.

Objective: The current study aims to comparatively investigate the antimicrobial potential and phytochemical compositions of citrus peel essential oils (EOs) and phenolic compounds (PCs) as an approach to combat life-threatening bacterial and fungal infections.

Methods: Citrus EOs and PCs were extracted from Citrus aurantifolia, Citrus reshni, Citrus latifolia and Citrus paradisi peels and phytochemically characterized by GC-MS and HPLC, respectively. The antimicrobial potential of citrus peel EOs and PCs was tested against Staphylococcus aureus, Bacillus cereus, Listeria monocytogenes, Escherichia coli O157:H7, Pseudomonas aeruginosa, Salmonella typhimurium and Candida albicans using disc diffusion and broth microdilution assays.

Results: The compositional analysis of citrus peel EOs revealed that limonene was the major volatile constituent, comprising 81.38%, 79.39%, 76.40% and 52.35% of grapefruit, mandarin, orange and lemon EOs, respectively. In addition, naringenin was the most abundant PC in grapefruit, orange and mandarin peel methanolic extracts, whereas catechin was the major PC in lemon peel. Lemon EO displayed the highest inhibitory effects against the investigated Gram-positive and Gram-negative bacteria as well as Candida albicans. Moreover, mandarin PCs exhibited the highest antibacterial effects, while orange PCs displayed the highest anticandidal effects. Furthermore, Gram-positive bacteria displayed higher sensitivity to both citrus peel EOs and PCs.

Conclusion: Citrus peel extracts possess versatile bioactive compounds that can be utilized as promising antimicrobial candidates.

Graphical Abstract

[1]
Gorlenko, C.L.; Kiselev, H.Y.; Budanova, E.V.; Zamyatnin, A.A., Jr; Ikryannikova, L.N. Plant secondary metabolites in the battle of drugs and drug-resistant bacteria: New heroes or worse clones of antibiotics? Antibiotics, 2020, 9(4), 170.
[http://dx.doi.org/10.3390/antibiotics9040170] [PMID: 32290036]
[2]
Zaman, S.B.; Hussain, M.A.; Nye, R.; Mehta, V.; Mamun, K.T.; Hossain, N. A review on antibiotic resistance: Alarm bells are ringing. Cureus, 2017, 9(6), e1403.
[http://dx.doi.org/10.7759/cureus.1403] [PMID: 28852600]
[3]
Global shortage of innovative antibiotics fuels emergence and spread of drug-resistance; World Health Organization, 2021. Available from: https://www.who.int/news/item/15-04-2021-global-shortage-of-innovative-antibiotics-fuels-emergence-and-spread-of-drug-resistance
[4]
Dadgostar, P. Antimicrobial resistance: Implications and costs. Infect. Drug Resist., 2019, 12, 3903-3910.
[http://dx.doi.org/10.2147/IDR.S234610] [PMID: 31908502]
[5]
Vaou, N.; Stavropoulou, E.; Voidarou, C.; Tsigalou, C.; Bezirtzoglou, E. Towards advances in medicinal plant antimicrobial activity: A review study on challenges and future perspectives. Microorganisms, 2021, 9(10), 2041.
[http://dx.doi.org/10.3390/microorganisms9102041] [PMID: 34683362]
[6]
El-Saadony, M.T.; Zabermawi, N.M.; Zabermawi, N.M.; Burollus, M.A.; Shafi, M.E.; Alagawany, M.; Yehia, N.; Askar, A.M.; Alsafy, S.A.; Noreldin, A.E.; Khafaga, A.F.; Dhama, K.; Elnesr, S.S.; Elwan, H.A.M.; Cerbo, A.D.; El-Tarabily, K.A.; Abd El-Hack, M.E. Nutri-tional aspects and health benefits of bioactive plant compounds against infectious diseases: A review. Food Rev. Int., 2021, 1-23.
[http://dx.doi.org/10.1080/87559129.2021.1944183]
[7]
Saini, R.K.; Ranjit, A.; Sharma, K.; Prasad, P.; Shang, X.; Gowda, K.G.M.; Keum, Y.S. Bioactive compounds of citrus fruits: A review of composition and health benefits of carotenoids, flavonoids, limonoids, and terpenes. Antioxidants, 2022, 11(2), 239.
[http://dx.doi.org/10.3390/antiox11020239] [PMID: 35204122]
[8]
Russo, C.; Maugeri, A.; Lombardo, G.E.; Musumeci, L.; Barreca, D.; Rapisarda, A.; Cirmi, S.; Navarra, M. The second life of Citrus fruit waste: A valuable source of bioactive compounds. Molecules, 2021, 26(19), 5991.
[http://dx.doi.org/10.3390/molecules26195991] [PMID: 34641535]
[9]
Wedamulla, N.E.; Fan, M.; Choi, Y.J.; Kim, E.K. Citrus peel as a renewable bioresource: Transforming waste to food additives. J. Funct. Foods, 2022, 95, 105163.
[http://dx.doi.org/10.1016/j.jff.2022.105163]
[10]
Lu, X.; Zhao, C.; Shi, H.; Liao, Y.; Xu, F.; Du, H.; Xiao, H.; Zheng, J. Nutrients and bioactives in citrus fruits: Different citrus varieties, fruit parts, and growth stages. Crit. Rev. Food Sci. Nutr., 2021, 1-24.
[http://dx.doi.org/10.1080/10408398.2021.1969891] [PMID: 34609268]
[11]
Behiry, S.I.; Okla, M.K.; Alamri, S.A.; EL-Hefny, M.; Salem, M.Z.M.; Alaraidh, I.A.; Ali, H.M.; Al-Ghtani, S.M.; Monroy, J.C.; Salem, A.Z.M. Antifungal and antibacterial activities of Musa paradisiaca L. peel extract: HPLC analysis of phenolic and flavonoid contents. Processes, 2019, 7(4), 215.
[http://dx.doi.org/10.3390/pr7040215]
[12]
Le, X.T.; Ha, P.T.H.; Phong, H.X.; Hien, T.T.; Ngan, T.T.K. Extraction of essential oils and volatile compounds of kaffir lime (Citrus hys-trix D.C) by hydrodistillation method. IOP Conf Ser Mater Sci Eng, 2020, pp. 18-23.
[http://dx.doi.org/10.1088/1757-899X/991/1/012024]
[13]
Middha, S.K.; Usha, T.; Pande, V. HPLC evaluation of phenolic profile, nutritive content, and antioxidant capacity of extracts obtained from Punica granatum fruit peel. Adv. Pharmacol. Sci., 2013, 2013, 1-6.
[http://dx.doi.org/10.1155/2013/296236] [PMID: 23983682]
[14]
Alsakhawy, S.A.; Baghdadi, H.H.; El-Shenawy, M.A.; Sabra, S.A.; El-Hosseiny, L.S. Encapsulation of thymus vulgaris essential oil in caseinate/gelatin nanocomposite hydrogel: In vitro antibacterial activity and in vivo wound healing potential. Int. J. Pharm., 2022, 628, 122280.
[http://dx.doi.org/10.1016/j.ijpharm.2022.122280] [PMID: 36243326]
[15]
Alsakhawy, S.A.; Baghdadi, H.H.; El-Shenawy, M.A.; El-Hosseiny, L.S. Antibacterial activity of silver nanoparticles phytosynthesized by citrus fruit peel extracts. Bionanoscience, 2022, 12(4), 1106-1115.
[http://dx.doi.org/10.1007/s12668-022-01030-9]
[16]
CLSI. Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically; Clinical and Laboratory Standards Institute, 2018, p. 91.
[17]
Ruiz-Pérez, N.J.; González-Ávila, M.; Sánchez-Navarrete, J.; Toscano-Garibay, J.D.; Moreno-Eutimio, M.A.; Sandoval-Hernández, T.; Arriaga-Alba, M. Antimycotic activity and genotoxic evaluation of Citrus sinensis and Citrus latifolia essential oils. Sci. Rep., 2016, 6(1), 25371.
[http://dx.doi.org/10.1038/srep25371] [PMID: 27137128]
[18]
Paw, M.; Begum, T.; Gogoi, R.; Pandey, S.K.; Lal, M. Chemical composition of Citrus limon L. burmf peel essential oil from North East India. J. Essent. Oil-Bear. Plants, 2020, 23(2), 337-344.
[http://dx.doi.org/10.1080/0972060X.2020.1757514]
[19]
Lin, X.; Cao, S.; Sun, J.; Lu, D.; Zhong, B.; Chun, J. The chemical compositions, and antibacterial and antioxidant activities of four types of citrus essential oils. Molecules, 2021, 26(11), 3412.
[http://dx.doi.org/10.3390/molecules26113412] [PMID: 34199966]
[20]
Caputo, L.; Cornara, L.; Bazzicalupo, M.; De Francesco, C.; De Feo, V.; Trombetta, D.; Smeriglio, A. Chemical composition and biological activities of essential oils from peels of three citrus species. Molecules, 2020, 25(8), 1890.
[http://dx.doi.org/10.3390/molecules25081890] [PMID: 32325864]
[21]
Kummer, R.; Fachini-Queiroz, F.C.; Estevão-Silva, C.F.; Grespan, R.; Silva, E.L.; Bersani-Amado, C.A.; Cuman, R.K.N. Evaluation of anti-inflammatory activity of Citrus latifolia Tanaka essential oil and limonene in experimental mouse models. Evid. Based Complement. Alternat. Med., 2013, 2013, 1-8.
[http://dx.doi.org/10.1155/2013/859083] [PMID: 23762165]
[22]
Sun, J.; Sun, P.; Kang, C.; Zhang, L.; Guo, L.; Kou, Y. Chemical composition and biological activities of essential oils from six lamiaceae folk medicinal plants. Plant-derived natural compounds in drug discovery: The prism perspective between plant phylogeny, chemical composi-tion, and medicinal efficacy. Front Plant Sci, 2023, 6648714, 78.
[http://dx.doi.org/10.3389/fpls.2022.919294]
[23]
Guimarães, A.C.; Meireles, L.M.; Lemos, M.F.; Guimarães, M.C.C.; Endringer, D.C.; Fronza, M.; Scherer, R. Antibacterial activity of terpenes and terpenoids present in essential oils. Molecules, 2019, 24(13), 2471.
[http://dx.doi.org/10.3390/molecules24132471] [PMID: 31284397]
[24]
Anagnostopoulou, M.A.; Kefalas, P.; Papageorgiou, V.P.; Assimopoulou, A.N.; Boskou, D. Radical scavenging activity of various extracts and fractions of sweet orange peel (Citrus sinensis). Food Chem., 2006, 94(1), 19-25.
[http://dx.doi.org/10.1016/j.foodchem.2004.09.047]
[25]
Abeysinghe, D.; Li, X.; Sun, C.; Zhang, W.; Zhou, C.; Chen, K. Bioactive compounds and antioxidant capacities in different edible tissues of citrus fruit of four species. Food Chem., 2007, 104(4), 1338-1344.
[http://dx.doi.org/10.1016/j.foodchem.2007.01.047]
[26]
Jabri karoui, I.; Marzouk, B. Characterization of bioactive compounds in tunisian bitter orange (Citrus aurantium L.) peel and juice and determination of their antioxidant activities. BioMed Res. Int., 2013, 2013, 1-12.
[http://dx.doi.org/10.1155/2013/345415]
[27]
Wang, H.; Chen, G.; Guo, X.; Abbasi, A.M.; Liu, R.H. Influence of the stage of ripeness on the phytochemical profiles, antioxidant and antiproliferative activities in different parts of Citrus reticulata Blanco cv. Chachiensis. Lebensm. Wiss. Technol., 2016, 69, 67-75.
[http://dx.doi.org/10.1016/j.lwt.2016.01.021]
[28]
Lü, Z.; Zhang, Z.; Wu, H.; Zhou, Z.; Yu, J. Phenolic composition and antioxidant capacities of chinese local pummelo cultivars’ peel. Hortic. Plant J., 2016, 2(3), 133-140.
[http://dx.doi.org/10.1016/j.hpj.2016.05.001]
[29]
Ferreira, S.S.; Silva, A.M.; Nunes, F.M. Citrus reticulata Blanco peels as a source of antioxidant and anti-proliferative phenolic compounds. Ind. Crops Prod., 2018, 111, 141-148.
[http://dx.doi.org/10.1016/j.indcrop.2017.10.009]
[30]
Liu, Y.; Benohoud, M.; Galani Yamdeu, J.H.; Gong, Y.Y.; Orfila, C. Green extraction of polyphenols from citrus peel by-products and their antifungal activity against Aspergillus flavus. Food Chem. X, 2021, 12, 100144.
[http://dx.doi.org/10.1016/j.fochx.2021.100144] [PMID: 34761200]
[31]
Kanaze, F.I.; Gabrieli, C.; Kokkalou, E.; Georgarakis, M.; Niopas, I. Simultaneous reversed-phase high-performance liquid chromato-graphic method for the determination of diosmin, hesperidin and naringin in different citrus fruit juices and pharmaceutical formulations. J. Pharm. Biomed. Anal., 2003, 33(2), 243-249.
[http://dx.doi.org/10.1016/S0731-7085(03)00289-9] [PMID: 12972089]
[32]
Gorinstein, S.; Haruenkit, R.; Park, Y.S.; Jung, S.T.; Zachwieja, Z.; Jastrzebski, Z.; Katrich, E.; Trakhtenberg, S.; Belloso, O.M. Bioactive compounds and antioxidant potential in fresh and dried Jaffa® sweeties, a new kind of citrus fruit. J. Sci. Food Agric., 2004, 84(12), 1459-1463.
[http://dx.doi.org/10.1002/jsfa.1800]
[33]
Long, X.; Zeng, X.; Yan, H.; Xu, M.; Zeng, Q.; Xu, C.; Xu, Q.; Liang, Y.; Zhang, J. Flavonoids composition and antioxidant potential as-sessment of extracts from Gannanzao Navel Orange (Citrus sinensis Osbeck Cv. Gannanzao) peel. Nat. Prod. Res., 2021, 35(4), 702-706.
[http://dx.doi.org/10.1080/14786419.2019.1593162] [PMID: 30942104]
[34]
Brahem, M.; Renard, C.M.G.C.; Eder, S.; Loonis, M.; Ouni, R.; Mars, M.; Le Bourvellec, C. Characterization and quantification of fruit phenolic compounds of European and Tunisian pear cultivars. Food Res. Int., 2017, 95, 125-133.
[http://dx.doi.org/10.1016/j.foodres.2017.03.002] [PMID: 28395820]
[35]
Jiménez-Moreno, N.; Volpe, F.; Moler, J.A.; Esparza, I.; Ancín-Azpilicueta, C. Impact of extraction conditions on the phenolic composition and antioxidant capacity of grape stem extracts. Antioxidants, 2019, 8(12), 597.
[http://dx.doi.org/10.3390/antiox8120597] [PMID: 31795232]
[36]
Zhang, J.; Wang, Y.; Yang, B.; Li, Y.; Liu, L.; Zhou, W.; Zheng, S.J. Profiling of phenolic compounds of fruit peels of different ecotype bananas derived from domestic and imported cultivars with different maturity. Horticulturae, 2022, 8(1), 70.
[http://dx.doi.org/10.3390/horticulturae8010070]
[37]
Hsouna, A.B.; Hamdi, N.; Halima, N.B.; Abdelkafi, S. Characterization of essential oil from Citrus aurantium L. flowers: antimicrobial and antioxidant activities. J. Oleo Sci., 2013, 62(10), 763-772.
[http://dx.doi.org/10.5650/jos.62.763] [PMID: 24088513]
[38]
Fancello, F.; Petretto, G.L.; Zara, S.; Sanna, M.L.; Addis, R.; Maldini, M.; Foddai, M.; Rourke, J.P.; Chessa, M.; Pintore, G. Chemical char-acterization, antioxidant capacity and antimicrobial activity against food related microorganisms of Citrus limon var. pompia leaf essential oil. Lebensm. Wiss. Technol., 2016, 69, 579-585.
[http://dx.doi.org/10.1016/j.lwt.2016.02.018]
[39]
Tran, T.K.N.; Ngo, T.C.Q.; Tran, T.H.; Bach, L.G.; Tran, T.T.; Huynh, X.P. Comparison of volatile compounds and antibacterial activity of Citrus aurantifolia, Citrus latifolia, and Citrus hystrix shell essential oils by pilot extraction. IOP Conf Ser Mater Sci Eng, 2021.
[http://dx.doi.org/10.1088/1757-899X/1092/1/012076]
[40]
Guo, J.; Gao, Z.; Xia, J.; Ritenour, M.A.; Li, G.; Shan, Y. Comparative analysis of chemical composition, antimicrobial and antioxidant activity of citrus essential oils from the main cultivated varieties in China. Lebensm. Wiss. Technol., 2018, 97, 825-839.
[http://dx.doi.org/10.1016/j.lwt.2018.07.060]
[41]
Upadhyay, R.K.; Dwivedi, P.; Ahmad, S. Screening of antibacterial activity of six plant essential oils against pathogenic bacterial strains. Asian J. Med. Sci., 2010, 2, 152-158.
[42]
Qadir, R.; Anwar, F.; Mehmood, T.; Shahid, M.; Zahoor, S. Variations in chemical composition, antimicrobial and haemolytic activities of peel essential oils from three local Citrus cultivars. Pure Appl. Biol., 2018, 7(1), 282-291.
[http://dx.doi.org/10.19045/bspab.2018.70034]
[43]
Teneva, D.; Denkova-Kostova, R.; Goranov, B.; Hristova-Ivanova, Y.; Slavchev, A.; Denkova, Z.; Kostov, G. Chemical composition, antioxidant activity and antimicrobial activity of essential oil from Citrus aurantium L zest against some pathogenic microorganisms. Z. Naturforsch. C J. Biosci., 2019, 74(5-6), 105-111.
[http://dx.doi.org/10.1515/znc-2018-0062] [PMID: 30685748]
[44]
Diao, W.R.; Hu, Q.P.; Feng, S.S.; Li, W.Q.; Xu, J.G. Chemical composition and antibacterial activity of the essential oil from green huajiao (Zanthoxylum schinifolium) against selected foodborne pathogens. J. Agric. Food Chem., 2013, 61(25), 6044-6049.
[http://dx.doi.org/10.1021/jf4007856] [PMID: 23758080]
[45]
Couladis, M.; Tzakou, O.; Kujundzic, S.; Sokovic, M.; Mimica-Dukic, N. Chemical analysis and antifungal activity of Thymus striatus. Phytother. Res., 2004, 18(1), 40-42.
[http://dx.doi.org/10.1002/ptr.1353] [PMID: 14750199]
[46]
Soković, M.; van Griensven, L.J.L.D. Antimicrobial activity of essential oils and their components against the three major pathogens of the cultivated button mushroom, Agaricus bisporus. Eur. J. Plant Pathol., 2006, 116(3), 211-224.
[http://dx.doi.org/10.1007/s10658-006-9053-0]
[47]
El-Hosseiny, L.; El-Shenawy, M.; Haroun, M.; Abdullah, F. Comparative evaluation of the inhibitory effect of some essential oils with antibiotics against Pseudomonas aeruginosa. Int. J. Antibiot., 2014, 2014, 1-5.
[http://dx.doi.org/10.1155/2014/586252]
[48]
Nazzaro, F.; Fratianni, F.; Coppola, R.; Feo, V.D. Essential oils and antifungal activity. Pharmaceuticals, 2017, 10(4), 86.
[http://dx.doi.org/10.3390/ph10040086] [PMID: 29099084]
[49]
Aljaafari, M.N.; AlAli, A.O.; Baqais, L.; Alqubaisy, M.; AlAli, M.; Molouki, A.; Ong-Abdullah, J.; Abushelaibi, A.; Lai, K.S.; Lim, S.H.E. An overview of the potential therapeutic applications of essential oils. Molecules, 2021, 26(3), 628.
[http://dx.doi.org/10.3390/molecules26030628] [PMID: 33530290]
[50]
Mancuso, M.; Catalfamo, M.; Laganà, P.; Rappazzo, A.C.; Raymo, V.; Zampino, D.; Zaccone, R. Screening of antimicrobial activity of citrus essential oils against pathogenic bacteria and Candida strains. Flavour Fragrance J., 2019, 34(3), 187-200.
[http://dx.doi.org/10.1002/ffj.3491]
[51]
Casquete, R.; Castro, S.M.; Martín, A.; Ruiz-Moyano, S.; Saraiva, J.A.; Córdoba, M.G.; Teixeira, P. Evaluation of the effect of high pres-sure on total phenolic content, antioxidant and antimicrobial activity of citrus peels. Innov. Food Sci. Emerg. Technol., 2015, 31, 37-44.
[http://dx.doi.org/10.1016/j.ifset.2015.07.005]
[52]
Naz, S.; Siddiqi, R.; Ahmad, S.; Rasool, S.A.; Sayeed, S.A. Antibacterial activity directed isolation of compounds from Punica granatum. J. Food Sci., 2007, 72(9), M341-M345.
[http://dx.doi.org/10.1111/j.1750-3841.2007.00533.x] [PMID: 18034726]
[53]
Shehata, M.G.; Awad, T.S.; Asker, D.; El Sohaimy, S.A. Abd El- Aziz, N.M.; Youssef, M.M. Antioxidant and antimicrobial activities and UPLC-ESI-MS/MS polyphenolic profile of sweet orange peel extracts. Curr. Res.Food Sci., 2021, 4, 326-335.
[http://dx.doi.org/10.1016/j.crfs.2021.05.001] [PMID: 34124691]
[54]
Li, Z.H.; Cai, M.; Liu, Y.S.; Sun, P.L.; Luo, S.L. Antibacterial activity and mechanisms of essential oil from Citrus medica L. var. sarcodactylis. Molecules, 2019, 24(8), 1577.
[http://dx.doi.org/10.3390/molecules24081577] [PMID: 31013583]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy