Antibacterial Properties of Leaves and Peels Extracts of Citrus aurantifolia cultivated in Algeria against Multi-Drug Resistant Staphylococcus aureus Originating from Raw Milk http://www.doi.org/10.26538/tjnpr/v7i10.20
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Abstract
Plants have an increased consumer preference and acceptability for the treatment of several diseases. Here, the antibacterial properties of organic extracts obtained from leaves and peels of Citrus aurantifolia from Algeria have been characterized. Two solvents, methanol, and ethanol, were employed to extract the bioactive components. Quantitative analysis of total phenols and flavonoids was conducted for the different extracts. The antibacterial activity was tested against multidrug-resistant Staphylococcus aureus strains originating from raw milk and reference strains including Escherichia coli ATCC 25922, Pseudomonas aeruginosa ATCC 27853, Staphylococcus aureus ATCC 25923, and Bacillus cereus ATCC 11778. The results revealed that leaves and peels extracts displayed significant antibacterial activity against the tested bacteria. The inhibition zone diameters observed ranged from 16.00 mm to 22.00 mm. The highest antimicrobial effect was observed with the ethanol extracts against the multidrug-resistant S. aureus strains, as indicated by a minimum inhibitory concentration of 1.56 mg/ml. The highest total phenolics and flavonoids contents were found to be 96 mg GAE/g and 54 mg QE/g in peels. Hence, the reported results unveil valuable insights into the antibacterial effects of Citrus aurantifolia extracts which have potential antimicrobial applications.
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El-Deeb W, Fayez M, Alhumam N, Elsohaby I, Quadri SA, Mkrtchyan H. The effect of staphylococcal mastitis including resistant strains on serum procalcitonin, neopterin, acute phase response and stress biomarkers in Holstein dairy cows. PeerJ. 2021; 9. doi: 10.7717/peerj.11511.
Liu H, Dong L, Zhao Y, Meng L, Wang J, Wang C, Zheng N. Antimicrobial susceptibility, and molecular characterization of Staphylococcus aureus isolated from different raw milk samples in China. Front Microbiol. 2022; 13: 840670. doi: 10.3389/fmicb.2022.840670.
Becker K, Skov RL, von Eiff C. Staphylococcus, Micrococcus, and other catalase-positive cocci. In: Pfaller MA, Carroll KC, Funke G, Landry ML, Richter SS, et al. (Eds.). Manual of Clinical Microbiology. Washington, DC: ASM Press; 2015. 354–382 p.
Tong SY, Davis JS, Eichenberger E, Holland TL, Fowler VG Jr. Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management. Clin Microbiol Rev. 2015; 28(3): 603-61. doi: 10.1128/CMR.00134-14.
Rai A, Khairnar K. Overview of the risks of Staphylococcus aureus infections and their control by bacteriophages and bacteriophage-encoded products. Braz J Microbiol. 2021; 52(4): 2031-2042. doi: 10.1007/s42770-021-00566-4.
Founou RC, Founou LL, Essack SY. Clinical and economic impact of antibiotic resistance in developing countries: a systematic review and meta-analysis. PLoS One. 2017; 12:e0189621. doi: 10.1371/journal.pone.0189621.
Bengtsson B, Unnerstad HE, Ekman T, Artursson K, Nilsson-Öst M, Waller KP. Antimicrobial susceptibility of udder pathogens from cases of acute clinical mastitis in dairy cows. Vet Microbiol. 2009; 136(1-2): 142-149. doi: 10.1016/j.vetmic.2008.10.024.
Ruegg PL, Oliveira L, Jin W, Okwumabua O. Phenotypic antimicrobial susceptibility and occurrence of selected resistance genes in gram-positive mastitis pathogens isolated from Wisconsin dairy cows. J Dairy Sci. 2015; 98(7): 4521-4534. doi: 10.3168/jds.2014-9137.
Kovačević Z, Samardžija M, Horvat O, Tomanić D, Radinović M, Bijelić K, Vukomanović AG, Kladar N. Is there a relationship between antimicrobial use and antibiotic resistance of the most common mastitis pathogens in dairy cows? Antibiotics. 2023; 12(1). doi: 10.3390/antibiotics12010003.
Rajput M, Kumar N. Medicinal plants: A potential source of novel bioactive compounds showing antimicrobial efficacy against pathogens infecting hair and scalp. Gene Rep. 2020; 21: 100879. doi:10.1016/j.genrep.2020.100879.
Reghu R, Sahadevan P, Sugathan S. Antimicrobial Agents from Plants. In: Sugathan S, Pradeep N, Abdulhameed S (Eds.). Bioresources and Bioprocess in Biotechnology. Springer, Singapore; 2017. 271-290 p. doi:10.1007/978-981-10-4284-3_11.
Gadisa E, Weldearegay G, Desta K, Tsegaye G, Hailu S, Jote K, Takele A. Combined antibacterial effect of essential oils from three most commonly used Ethiopian traditional medicinal plants on multidrug resistant bacteria. BMC Complement. Altern. Med. 2019; 19(24): 1-9.
Anwar F, Naseer R, Bhanger MI, Ashraf S, Talpur FN, Aladedunye FA. Physico-chemical characteristics of citrus seeds and seed oils from Pakistan. JAOCS. 2008; 85(4): 321-330. doi:10.1007/s11746-008-1204-3.
Food and Agriculture Organization of the United Nations (FAO) FAOSTAT. Crops and livestock products. [Online]. 2020 [Cited 2023 July 13] Available from: https://www.fao.org/faostat/en/#data/QCL [Cited 2023 July 13].
Andrade MA, Barbosa CH, Shah MA, Ahmad N, Vilarinho F, Khwaldia K, Silva AS, Ramos F. Citrus by-products: valuable source of bioactive compounds for food applications. Antioxidants. 2023; 12(38). doi: 10.3390/antiox12010038.
Mahato N, Sinha M, Sharma K, Koteswararao R, Cho MH. Modern extraction and purification techniques for obtaining high purity food-grade bioactive compounds and value-added co-products from citrus wastes. Foods. 2019; 8: 523. doi:10.3390/foods8110523.
Panwar D, Saini A, Panesar PS, Chopra HK. Unraveling the scientific perspectives of citrus by-products utilization: Progress towards circular economy. Trends Food Sci Technol. 2021; 111: 549-562. doi:10.1016/j.tifs.2021.03.018.
Abayomi OJ, Oyewole AO, Olagunju JA, Akinola OO, Omotosho OE. Curative Effect of Aqueous Seed Extract of Citrus paradisi against Carbon Tetrachloride-Induced Nephrotoxicity in Wistar Rats. TJNPR. 2021; 5(4): 749–752. doi.org/10.26538/tjnpr/v5i4.25.
Laksemi DA, Tunas K, A Damayanti PA, Sudarmaja IM, Widyadharma IPE, D Wiryanthini IA, Linawati NM. Evaluation of antimalarial activity of combination extract of Citrus aurantifolia and honey against Plasmodium berghei–İnfected mice. TJNPR. 2023; 7(1): 2168–2171. doi: 10.26538/tjnpr/v7i1.13.
Shorinwa OA, Otu VS. Immunomodulatory activity of the aqueous extract of the pith of Citrus limon L. (Rutaceae) using cyclophosphamide induced myelosuppression. TJNPR. 2023; 7(3): 2660–2664. doi: 10.26538/tjnpr/v7i3.29.
Bellavite P, Donzelli A. Hesperidin and SARS-CoV-2: New Light on the Healthy Function of Citrus Fruits. Antioxidants. 2020; 9(8):742. https://doi.org/10.3390/antiox9080742
Nakajima A, Ohizumi Y. Potential benefits of nobiletin, a citrus flavonoid, against Alzheimer’s disease and Parkinson’s disease. Int J Mol Sci. 2019; 20(14): 3380. https://doi.org/10.3390/ijms20143380
Goh JXH, Tan LT-H, Goh JK, Chan KG, Pusparajah P, Lee L-H, Goh B-H. Nobiletin and Derivatives: Functional compounds from citrus fruit peel for colon cancer chemoprevention. Cancers. 2019; 11(6): 867. https://doi.org/10.3390/cancers11060867
Lemes RS, Alves CCF, Estevam EBB, Santiago MB, Martins CHG, Santos TCLD, Crotti AEM, Miranda MLD. Chemical composition and antibacterial activity of essential oils from Citrus aurantifolia leaves and fruit peel against oral pathogenic bacteria. An Acad Bras Cienc. 2018; 90(2): 1285-1292. doi: 10.1590/0001-3765201820170847.
El-Desoukey RMA, Saleh ASB, Alhowamil HF. The phytochemical and antimicrobial effect of Citrus sinensis (Orange) peel powder extracts on some animal pathogens as eco-friendly. EC Microbiol. 2018; 14(6): 312-318.
Bambeni T, Tayengwa T, Chikwanha OC, Manley M, Gouws PA, Marais J, Fawole OA, Mapiye C. Biopreservative efficacy of grape (Vitis vinifera) and clementine mandarin orange (Citrus reticulata) by-product extracts in raw ground beef patties. Meat Sci. 2021; 181: 108609. doi: 10.1016/j.meatsci.2021.108609.
Torimiro N, Adegun B, Abioye O, Omole R. Antibacterial activity of essential oil from Citrus aurantifolia (Christm.) Swingle peels against multidrug-resistant bacterial isolates. AIM. 2020; 10: 214-223. doi: 10.4236/aim.2020.105017.
Evy Ratnasari Ekawati, Windarmanto, Sri Puji Astuti Wahyuningsih. Study of lime peel flavonoid as effectively antibacterial against Methicillin-resistant Staphylococcus aureus. RJPT. 2022; 15(7): 3002-8. doi: 10.52711/0974-360X.2022.00501
CLSI, 2020. Performance standards for antimicrobial susceptibility testing. 30th ed. CLSI Supplement M100. Wayne, PA: Clinical Laboratory Standards Institute; 2020.
National Committee for Clinical Laboratory Standards (NCCLS). Performance standard for antimicrobial disc susceptibility tests. Approved standard. NCCLS document M2-A5. Wayne, Pa: National Committee for Clinical Laboratory Standards; 1993.
Arruda HS, Pereira GA, Pastore GM. Optimization of extraction parameters of total phenolics from Annona crassiflora Mart. (Araticum) fruits using response surface methodology. Food Anal Methods. 2017; 10(1): 100-110. doi:10.1007/s12161-016-0554-y.
Phuyal N, Jha PK, Raturi PP, Rajbhandary S. Total phenolic, flavonoid contents, and antioxidant activities of fruit, seed, and Bark extracts of Zanthoxylum armatum DC. Sci World J. 2020; 2020. doi: 10.1155/2020/8780704.
Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, Harbarth S, Hindler JF, Kahlmeter G, Olsson-Liljequist B, Paterson DL, Rice LB, Stelling J, Struelens MJ, Vatopoulos A, Weber JT, Monnet DL. Multidrug-resistant, extensively drug-resistant and pan drug-resistant bacteria: An international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012; 18(3): 268-281. doi: 10.1111/j.1469-0691.2011.03570.x.
Wendlandt S, Feßler AT, Monecke S, Ehricht R, Schwarz S, Kadlec K. The diversity of antimicrobial resistance genes among staphylococci of animal origin. Int J Med Microbiol. 2013; 303(6-7): 338-349. doi: 10.1016/j.ijmm.2013.02.006.
Mestrovic T, Robles Aguilar G, Swetschinski LR, et al. The burden of bacterial antimicrobial resistance in the WHO European region in 2019: a cross-country systematic analysis. Lancet Public Health. 2022; 7(11): e897-e913. doi:10.1016/S2468-2667(22)00225-0.
Lee JH, Cho S, Paik HD, Choi CW, Nam KT, Hwang SG, Kim SK. Investigation on antibacterial and antioxidant activities, phenolic and flavonoid contents of some Thai edible plants as an alternative for antibiotics. Asian-Australas J Anim Sci. 2014; 27(10): 1461-1468. doi: 10.5713/ajas.2013.13629.
Phattayakorn K, Wanchaitanawong P. Antimicrobial activity of Thai herb extracts against coconut milk spoilage microorganisms. Nat Sci. 2009; 43: 752-759.
Shakya A, Luitel B, Kumari P, Devkota R, Dahal PR, Chaudhary R. Comparative study of antibacterial activity of juice and peel extract of Citrus fruits. TUJM. 2019; 6: 82-88. doi:10.3126/tujm.v6i0.26589.
Abdallah EM. Preliminary phytochemical and antibacterial screening of methanolic leaf extract of Citrus aurantifolia. Pharm Biotechnol Curr Res. 2016; 1:1.
Rawat S, Jugran AK, Bahukhandi A, Bahuguna A, Bhatt ID, Rawal RS, Dhar U. Anti-oxidant and anti-microbial properties of some ethno-therapeutically important medicinal plants of Indian Himalayan Region. 3 Biotech. 2016; 6:154. doi: 10.1007/s13205-016-0470-2. Epub 2016 Jul 18.
Ouerghemmi I, Bettaieb Rebey I, Rahali FZ, Bourgou S, Pistelli L, Ksouri R, Marzouk B, Tounsi MS. Antioxidant and antimicrobial phenolic compounds from extracts of cultivated and wild-grown Tunisian Ruta chalepensis. J Food Drug Anal. 2017; 25(2): 350-359. doi: 10.1016/j.jfda.2016.04.001.
Inouye S, Yamaguchi H, Takizawa T, Inouye S, Yamaguchi · H, Takizawa T. Screening of the antibacterial effects of a variety of essential oils on respiratory tract pathogens, using a modified dilution assay method. J Infect Chemother. 2001; 7: 251-254. doi: 10.1007/s101560170022.
Al Ubeed HMS, Bhuyan DJ, Alsherbiny MA, Basu A, Vuong Q V. A comprehensive review on the techniques for extraction of bioactive compounds from medicinal Cannabis. Molecules. 2022; 27: 604. doi:10.3390/molecules27030604.
Akinmoladun AC, Falaiye OE, Ojo OB, Adeoti A, Amoo ZA, Olaleye MT. Effect of extraction technique, solvent polarity, and plant matrix on the antioxidant properties of Chrysophyllum albidum G. Don (African Star Apple). Bull Natl Res Cent. 2022; 46(1). doi:10.1186/s42269-022-00718-y.
Pasaribu F, Ervina I, Suryanto D. The effectiveness antimicrobial activity test of citrus peel extract on some periodontal pathogenic bacteria (In vitro). Int J Appl Dent Sci. 2018; 4(3): 146-150.
Singhapol C, Tinrat S. Virulence genes analysis of Vibrio parahaemolyticus and anti-Vibrio activity of the citrus extracts. Curr Microbiol. 2020; 77(8): 1390-1398. doi:10.1007/s00284-020-01941-4.
Munawaroh R, Yani JA, Pos T, Kartasura P. Optimum conditions for extraction of antibacterial compounds from Citrus aurantifolia fruit peel waste. PHA. 2017; 18: 34-38.
Rumzum Bhuiyan F, Hasan M, Abdus Shukur Imran M, Rashel Ahmed S, Shukur Imran A, Shanzana P. Antimicrobial activity screening for three Citrus pulp extracts and phytochemical constituency profiling. J Pharmacogn Phytochem. 2019; 8(4): 157-161.
Ugwu CC, Mbah-Omeje KN, Ezeugwu RI, Onuorah SC, Agbo MC. Antimicrobial activities and phytochemical screening of Citrus aurantifoila (Lime) leaf extracts and fruit juice on some microorganisms. IJIRD. 2018; 7(3). doi:10.24940/ijird/2018/v7/i3/mar18031.
Zage AZ, Tajo S, Ali M. Antibacterial activity of Citrus aurantifolia leaves extracts against some enteric bacteria of public health importance. MAMS. 2018; 1(2): 33-38. doi:10.32474/mams.2018.01.000107.
Rafiq S, Kaul R, Sofi SA, Bashir N, Nazir F, Ahmad Nayik G. Citrus peel as a source of functional ingredient: A review. J Saudi Soc Agric Sci. 2018; 17(4): 351-358. doi:10.1016/j.jssas.2016.07.006.
Bouarab-Chibane L, Forquet V, Lantéri P, Clément Y, Léonard-Akkari L, Oulahal N, Degraeve P, Bordes C. Antibacterial properties of polyphenols: Characterization and QSAR (Quantitative structure-activity relationship) models. Front Microbiol. 2019; 10: 829. doi:10.3389/fmicb.2019.00829.
Efenberger-Szmechtyk M, Nowak A, Czyzowska A. Plant extracts rich in polyphenols: antibacterial agents and natural preservatives for meat and meat products. Crit Rev Food Sci Nutr. 2021; 61(1): 149-178. doi: 10.1080/10408398.2020.1722060.
Xie Y, Yang W, Tang F, Chen X, Ren L. Antibacterial activities of flavonoids: structure-activity relationship and mechanism. Curr Med Chem. 2014; 22(1): 132-149. doi: 10.2174/0929867321666140916113443.