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Current Pharmaceutical Biotechnology

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ISSN (Print): 1389-2010
ISSN (Online): 1873-4316

Research Article

The Phytochemical and Pharmacological Properties of Citrus sinensis ‘Maltese Half-blood’ Essential Oil Peels Extracted and Optimized by Response-surface Methodology

Author(s): Imen Kallel*, Nidhal Tarhouni, Asma Elaguel, Saoussen Mekrazi, Abdelmajid Khabir, Bilel Hadrich and Ahmed Bayoudh

Volume 24, Issue 15, 2023

Published on: 03 May, 2023

Page: [1938 - 1951] Pages: 14

DOI: 10.2174/1389201024666230405120520

Price: $65

Abstract

Background: Citrus fruits have been a valuable economic crop for thousands of years. Furthermore, citrus essential oils are significant in the perfume, food, and beverage sectors, as well as aromatherapy and medical medicines.

Aims: The present study aims to evaluate the phytochemical and pharmacological potentials of the optimized Citrus sinensis ‘Maltese half-blood’ essential oils peels (CsEO) extraction yields using Response-Surface Methodology (RSM).

Objective: There have been few investigations on Citrus sinensis ‘Maltese half-blood’ essential oil.

Methods: Citrus sinensis ‘Maltese half-blood’ essential oil peels (CsEO) extraction yields were performed by hydro-distillation and optimized by using Response-Surface Methodology (RSM). The oils were analysed by GC-MS. Different chemical tests were used to evaluate antioxidant activities. The healing potential was evaluated using models’ wounds on Wistar rats.

Results: The RSM optimization demonstrated the highest yield of CsEO of 6.89 g/100 g d.b. All three tested factors significantly influenced the CsEO extraction yield: washing saline solution concentration, washings number, and drying percentage of peels. Significant antioxidant activities were noted in CsEO: the DPPH assay reported an IC50 of 0.225 ± 0.014 mL/mg, the FRAP assay showed an IC50 of 0.235 ± 0.001, and the NO assay was an IC50 in order of 0.259 ± 0.019. CsEO was not genotoxic and considerably decreased the levels of DNA lesions induced by oxidants. Also, applying a cream with CsEO on wounds promotes significantly rapid wound healing.

Conclusion: CsEO could be considered a rich natural source of antioxidants and bio-compounds to accelerate wound healing. It can be used in pharmaceutical sectors as an alternative to synthetic chemicals.

Keywords: Essential oils, RSM, Citrus sinensis, antioxidant activity, DNA damage protection, wound healing.

Graphical Abstract
[1]
Carbone, C.; Martins-Gomes, C.; Caddeo, C.; Silva, A.M.; Musumeci, T.; Pignatello, R.; Puglisi, G.; Souto, E.B. Mediterranean essential oils as precious matrix components and active ingredients of lipid nanoparticles. Int. J. Pharm., 2018, 548(1), 217-226.
[http://dx.doi.org/10.1016/j.ijpharm.2018.06.064] [PMID: 29966744]
[2]
Rassem, H.; Nour, A. Techniques for extraction of essential oils from plants: A review. Aust. J. Basic Appl. Sci., 2016, 10, 117-127.
[3]
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.
[4]
Satari, B.; Karimi, K. Citrus processing wastes: Environmental impacts, recent advances, and future perspectives in total valorization. Resour. Conserv. Recycling, 2018, 129, 153-167.
[http://dx.doi.org/10.1016/j.resconrec.2017.10.032]
[5]
Zandalinas, S.I.; Sales, C.; Beltrán, J.; Gómez-Cadenas, A.; Arbona, V. Activation of secondary metabolism in citrus plants is associated to sensitivity to combined drought and high temperatures. Front. Plant Sci., 2017, 7, 1954.
[http://dx.doi.org/10.3389/fpls.2016.01954] [PMID: 28119698]
[6]
Favela-Hernández, J.; González-Santiago, O.; Ramírez-Cabrera, M.; Esquivel-Ferriño, P.; Camacho-Corona, M. Chemistry and Pharmacology of Citrus sinensis. Molecules, 2016, 21(2), 247.
[http://dx.doi.org/10.3390/molecules21020247] [PMID: 26907240]
[7]
Metoui, N.; Hamrouni, L.; Dhaoudi, F.; Bettaieb, T. Notes ethnobotanique et phytopharmacologique sur la Maltaise de Tunisie. Phytotherapie, 2014, 12(2), 105-108.
[http://dx.doi.org/10.1007/s10298-014-0856-4]
[8]
FAO. Food and Agriculture Organization of the United Nations; The State of Food and Agriculture, 2012.
[9]
Perini, J.F.; Silvestre, W.P.; Agostini, F.; Toss, D.; Pauletti, G.F. Fractioning of orange (Citrus sinensis L.) essential oil using vacuum fractional distillation. Sep. Sci. Technol., 2017, 52(8), 1397-1403.
[http://dx.doi.org/10.1080/01496395.2017.1290108]
[10]
Dao, T.P.; Quyen, N.T.C.; Nhi, T.T.Y.; Nguyen, C.C.; Nguyen, T.T.; Le, X.T. Response surface methodology for optimization studies of hydro-distillation of essential oil from pixie mandarin (Citrus reticulata Blanco) peels. Pol. J. Chem. Technol., 2021, 23(4), 26-34.
[http://dx.doi.org/10.2478/pjct-2021-0034]
[11]
Li, G.; Liu, S.; Zhou, Q.; Han, J.; Qian, C.; Li, Y.; Meng, X.; Gao, X.; Zhou, T.; Li, P.; Gu, Q. Effect of response surface methodology-optimized ultrasound-assisted pretreatment extraction on the composition of essential oil released from Tribute citrus Peels. Front. Nutr., 2022, 9, 840780.
[http://dx.doi.org/10.3389/fnut.2022.840780] [PMID: 35571948]
[12]
Kallel, I.; Bayoudh, A.; Gargouri, B.; Khannous, L.; Elaguel, A.; Tarhouni, N.; Lassoued, S.; Ben Messaoud, E.; Hadrich, B. Modeling of antiproliferative effects of Salvia officinalis L. essential oil optimized using Box-Behnken design. J. Plant Biochem. Biotechnol., 2022, 2022(1), 1-14.
[http://dx.doi.org/10.1007/s13562-022-00799-w]
[13]
Elaguel, A.; Kallel, I.; Gargouri, B.; Ben Amor, I.; Hadrich, B.; Ben Messaoud, E.; Gdoura, R.; Lassoued, S.; Gargouri, A. Lawsonia inermis essential oil: Extraction optimization by RSM, antioxidant activity, lipid peroxydation and antiproliferative effects. Lipids Health Dis., 2019, 18(1), 196.
[http://dx.doi.org/10.1186/s12944-019-1141-1] [PMID: 31727081]
[14]
Prieto, P.; Pineda, M.; Aguilar, M. Spectrophotometric quantitation of antioxidant capacity through the formation of a phosphomolybdenum complex: Specific application to the determination of vitamin E. Anal. Biochem., 1999, 269(2), 337-341.
[http://dx.doi.org/10.1006/abio.1999.4019] [PMID: 10222007]
[15]
Osawa, T.; Namiki, M. A novel type of antioxidant isolated from leaf wax ofeucalyptusleaves. Agric. Biol. Chem., 1981, 45(3), 735-739.
[http://dx.doi.org/10.1080/00021369.1981.10864583]
[16]
Kallel, I.; Hadrich, B.; Gargouri, B.; Chaabane, A.; Lassoued, S.; Gdoura, R.; Bayoudh, A.; Ben Messaoud, E. Optimization of cinnamon (Cinnamomum zeylanicum Blume) essential oil extraction: Evaluation of antioxidant and antiproliferative effects. Evid. Based Complement. Alternat. Med., 2019, 2019, 6498347.
[http://dx.doi.org/10.1155/2019/6498347] [PMID: 31929818]
[17]
Marcocci, L.; Maguire, J.J.; Droylefaix, M.T.; Packer, L. The nitric oxide-scavenging properties of Ginkgo biloba extract EGb 761. Biochem. Biophys. Res. Commun., 1994, 201(2), 748-755.
[http://dx.doi.org/10.1006/bbrc.1994.1764] [PMID: 8003011]
[18]
Benzie, I.F.F.; Strain, J.J. Ferric reducing/antioxidant power assay: Direct measure of total antioxidant activity of biological fluids and modified version for simultaneous measurement of total antioxidant power and ascorbic acid concentration. Methods Enzymol., 1999, 299, 15-27.
[http://dx.doi.org/10.1016/S0076-6879(99)99005-5] [PMID: 9916193]
[19]
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]
[20]
Zarai, Z.; Kadri, A.; Ben Chobba, I.; Ben Mansour, R.; Bekir, A.; Mejdoub, H.; Gharsallah, N. The in-vitro evaluation of antibacterial, antifungal and cytotoxic properties of Marrubium vulgare L. essential oil grown in Tunisia. Lipids Health Dis., 2011, 10(1), 161.
[http://dx.doi.org/10.1186/1476-511X-10-161] [PMID: 21936887]
[21]
Shukla, R.; Kashaw, V. Extraction and wound healing potential of Nerium Indicum M, Artocarpus Heterophyllus Lam, Murraya Koenigii L, Punica Granatum L on albino rats using burn wound model. J. Drug Deliv. Ther., 2019, 9(1-s), 337-346.
[http://dx.doi.org/10.22270/jddt.v9i1-s.2360]
[22]
Wu, Z.; Tang, Y.; Fang, H.; Su, Z.; Xu, B.; Lin, Y.; Zhang, P.; Wei, X. RETRACTED ARTICLE: Decellularized scaffolds containing hyaluronic acid and EGF for promoting the recovery of skin wounds. J. Mater. Sci. Mater. Med., 2015, 26(1), 59.
[http://dx.doi.org/10.1007/s10856-014-5322-1] [PMID: 25604697]
[23]
Cardiff, R.D.; Miller, C.H.; Munn, R.J. Manual hematoxylin and eosin staining of mouse tissue sections. Cold Spring Harb. Protoc, 2014, 2014(6), 655-658.
[http://dx.doi.org/10.1101/pdb.prot073411]
[24]
Golla, U.; Bhimathati, S.S.R. Evaluation of antioxidant and DNA damage protection activity of the hydroalcoholic extract of Desmostachya bipinnata L. Stapf. Sci. World J., 2014, 2014, 215084.
[http://dx.doi.org/10.1155/2014/215084] [PMID: 24574873]
[25]
Liu, K.; Deng, W.; Hu, W.; Cao, S.; Zhong, B.; Chun, J. Extraction of ‘Gannanzao’ orange peel essential oil by response surface methodology and its effect on cancer cell proliferation and migration. Molecules, 2019, 24(3), 499.
[http://dx.doi.org/10.3390/molecules24030499] [PMID: 30704118]
[26]
Fakayode, O.A.; Abobi, K.E. Optimization of oil and pectin extraction from orange (Citrus sinensis) peels: a response surface approach. J. Anal. Sci. Technol., 2018, 9(1), 20.
[http://dx.doi.org/10.1186/s40543-018-0151-3]
[27]
Kamal, G.M.; Anwar, F.; Hussain, A.I.; Sarri, N.; Ashraf, M.Y. Yield and chemical composition of Citrus essential oils as affected by drying pretreatment of peels. Int. Food Res. J., 2011, 18, 1275-1282.
[28]
Hosni, K.; Zahed, N.; Chrif, R.; Abid, I.; Medfei, W.; Kallel, M.; Brahim, N.B.; Sebei, H. Composition of peel essential oils from four selected Tunisian Citrus species: Evidence for the genotypic influence. Food Chem., 2010, 123(4), 1098-1104.
[http://dx.doi.org/10.1016/j.foodchem.2010.05.068]
[29]
Farhat, I.; Hammami, M.; Cherif, M.; Nasraoui, B. Chemometric analysis of geographic origins and compositions of Citrus sinensis (L.) Osbeck var ‘Maltaise demi sanguine’essential oil. J. Essent. Oil Res., 2020, 32(3), 216-226.
[http://dx.doi.org/10.1080/10412905.2020.1733110]
[30]
Bourgou, S.; Rahali, F.Z.; Ourghemmi, I.; Saïdani Tounsi, M. Changes of peel essential oil composition of four Tunisian citrus during fruit maturation. Sci. World J., 2012, 2012, 528593.
[http://dx.doi.org/10.1100/2012/528593] [PMID: 22645427]
[31]
Zouaghi, G.; Najar, A.; Chiboub, O.; Sifaoui, I.; Abderrabba, M.; Lorenzo Morales, J. The effect of viroid infection of citrus trees on the amoebicidal activity of ‘Maltese half-blood’ (Citrus sinensis) against trophozoite stage of Acanthamoeba castellanii Neff. Exp. Parasitol., 2017, 183, 182-186.
[http://dx.doi.org/10.1016/j.exppara.2017.09.006] [PMID: 28916460]
[32]
Şanli, A.; Karadoğan, T. Geographical impact on essential oil composition of endemickundmanniaanatolicahub.-mor.(APIACEAE). Afr. J. Tradit. Complement. Altern. Med., 2016, 14(1), 131-137.
[http://dx.doi.org/10.21010/ajtcam.v14i1.14] [PMID: 28480390]
[33]
Farhadi, N.; Babaei, K.; Farsaraei, S.; Moghaddam, M.; Ghasemi Pirbalouti, A. Changes in essential oil compositions, total phenol, flavonoids and antioxidant capacity of Achillea millefolium at different growth stages. Ind. Crops Prod., 2020, 152, 112570.
[http://dx.doi.org/10.1016/j.indcrop.2020.112570]
[34]
Kademi, H.I.; Garba, U. Citrus peel essential oils: A review on composition and antimicrobial activities. Nutr. Public Heal. Technol., 2017, 9, 38-44.
[35]
Sarrou, E.; Chatzopoulou, P.; Dimassi-Theriou, K.; Therios, I. Volatile constituents and antioxidant activity of peel, flowers and leaf oils of Citrus aurantium L. growing in Greece. Molecules, 2013, 18(9), 10639-10647.
[http://dx.doi.org/10.3390/molecules180910639] [PMID: 24002139]
[36]
Gómez-Mejía, E.; Rosales-Conrado, N.; León-González, M.E.; Madrid, Y. Citrus peels waste as a source of value-added compounds: Extraction and quantification of bioactive polyphenols. Food Chem., 2019, 295, 289-299.
[http://dx.doi.org/10.1016/j.foodchem.2019.05.136] [PMID: 31174761]
[37]
Himed, L.; Merniz, S.; Monteagudo-Olivan, R.; Barkat, M.; Coronas, J. Antioxidant activity of the essential oil of citrus limon before and after its encapsulation in amorphous SiO2. Sci. Am., 2019, 6, e00181.
[http://dx.doi.org/10.1016/j.sciaf.2019.e00181]
[38]
Crespo, Y.A.; Bravo Sánchez, L.R.; Quintana, Y.G.; Cabrera, A.S.T.; Bermúdez del, S.A.; Mayancha, D.M.G. Evaluation of the synergistic effects of antioxidant activity on mixtures of the essential oil from Apium graveolens L., Thymus vulgaris L. and Coriandrum sativum L. using simplex-lattice design. Heliyon, 2019, 5(6), e01942.
[http://dx.doi.org/10.1016/j.heliyon.2019.e01942] [PMID: 31245650]
[39]
Pereira, A.; Maraschin, M. Banana (Musa spp) from peel to pulp: Ethnopharmacology, source of bioactive compounds and its relevance for human health. J. Ethnopharmacol., 2015, 160, 149-163.
[http://dx.doi.org/10.1016/j.jep.2014.11.008] [PMID: 25449450]
[40]
Khan, A.; Ahmad, A.; Ahmad, K.L.; Padoa, C.J.; van Vuuren, S.; Manzoor, N. Effect of two monoterpene phenols on antioxidant defense system in Candida albicans. Microb. Pathog., 2015, 80, 50-56.
[http://dx.doi.org/10.1016/j.micpath.2015.02.004] [PMID: 25681060]
[41]
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]
[42]
Ramasamy, S.S.; Bhaskar, A. Evaluation of the wound-healing potency of Citrus sinensis in Wistar albino rats. Pharm. Lett., 2016, 8, 161-168.
[43]
Dahmani, S.; Chabir, R.; Errachidi, F.; Berrada, W.; Lansari, H.; Benidir, M.; El Ghadraoui, L.; Bour, A. Evaluation of in vivo wound healing activity of Moroccan Citrus reticulata peel extract. Clinical Phytoscience, 2020, 6(1), 78.
[http://dx.doi.org/10.1186/s40816-020-00222-8]
[44]
Gül Satar, N.Y.; Cangül, İ.T.; Topal, A.; Oktay, A.; İnan, K.; Akgül, M.B. Ankaferd Blood Stopper (ABS) ve topikal tripeptid baki{dotless}r kompleksinin (TCC) ratlarda yara İyileşmesi üzerine etkisi: Deneysel çali{dotless}şma. Kafkas Univ. Vet. Fak. Derg., 2014, 20, 545-551.
[http://dx.doi.org/10.9775/kvfd.2013.10555]
[45]
Sibbald, R.G.; Orsted, H.L.; Coutts, P.M.; Keast, D.H. Best practice recommendations for preparing the wound bed: Update 2006. Adv. Skin Wound Care, 2007, 20(7), 390-405.
[http://dx.doi.org/10.1097/01.ASW.0000280200.65883.fd] [PMID: 17620740]
[46]
Dosoky, N.; Setzer, W. Biological activities and safety of citrus spp. Essential oils. Int. J. Mol. Sci., 2018, 19(7), 1966.
[http://dx.doi.org/10.3390/ijms19071966] [PMID: 29976894]
[47]
Ishfaq, M.; Akhtar, B.; Muhammad, F.; Sharif, A.; Akhtar, M.F.; Hamid, I.; Sohail, K.; Muhammad, H. Antioxidant and wound healing potential of essential oil from Citrus reticulata peel and its chemical characterization. Medicinal values of peels essential oil. Curr. Pharm. Biotechnol., 2020, 21, 1114-1121.
[http://dx.doi.org/10.2174/1389201021999200918102123] [PMID: 32957881]
[48]
Ahmad, M.; Khan, T.H.; Ansari, M.N.; Ahmad, S.F. Enhanced wound healing by topical administration of d-limonene in alloxan induced diabetic mice through reduction of pro-inflammatory markers and chemokine expression. BMC Genomics, 2014, 15(S2), P29.
[http://dx.doi.org/10.1186/1471-2164-15-S2-P29]
[49]
Keskin, I.; Gunal, Y.; Ayla, S.; Kolbasi, B.; Sakul, A.; Kilic, U.; Gok, O.; Koroglu, K.; Ozbek, H. Effects of Foeniculum vulgare essential oil compounds, fenchone and limonene, on experimental wound healing. Biotech. Histochem., 2017, 92(4), 274-282.
[http://dx.doi.org/10.1080/10520295.2017.1306882] [PMID: 28426256]
[50]
Mazutti da Silva, S.; Rezende Costa, C.; Martins Gelfuso, G.; Silva Guerra, E.; de Medeiros Nóbrega, Y.; Gomes, S.; Pic-Taylor, A.; Fonseca-Bazzo, Y.; Silveira, D.; Magalhães, P. Wound healing effect of essential oil extracted from Eugenia dysenterica DC (Myrtaceae) leaves. Molecules, 2018, 24(1), 2.
[http://dx.doi.org/10.3390/molecules24010002] [PMID: 30577426]
[51]
Koyama, S.; Purk, A.; Kaur, M.; Soini, H.A.; Novotny, M.V.; Davis, K.; Kao, C.C.; Matsunami, H.; Mescher, A.; Cheng Kao, C.; Matsunami, H.; Mescher, A. Beta-caryophyllene enhances wound healing through multiple routes. PLoS One, 2019, 14(12), e0216104.
[http://dx.doi.org/10.1371/journal.pone.0216104] [PMID: 31841509]
[52]
Amorim, J.L.; Simas, D.L.R.; Pinheiro, M.M.G.; Moreno, D.S.A.; Alviano, C.S.; da Silva, A.J.R.; Dias Fernandes, P. Antiinflammatory properties and chemical characterization of the essential oils of four Citrus species. PLoS One, 2016, 11(4), e0153643.
[http://dx.doi.org/10.1371/journal.pone.0153643] [PMID: 27088973]
[53]
Prakash, D.; Singh, B.N.; Upadhyay, G. Antioxidant and free radical scavenging activities of phenols from onion (Allium cepa). Food Chem., 2007, 102(4), 1389-1393.
[http://dx.doi.org/10.1016/j.foodchem.2006.06.063]
[54]
Salehi, F.; Behboudi, H.; Kavoosi, G.; Ardestani, S.K. Oxidative DNA damage induced by ROS-modulating agents with the ability to target DNA: A comparison of the biological characteristics of citrus pectin and apple pectin. Sci. Reports, 2018, 81(8), 1-16.
[http://dx.doi.org/10.1038/s41598-018-32308-2]

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