ANTIBACTERIAL ACTIVITY OF AN ETHANOLIC EXTRACT DERIVED FROM LEAVES OF FICUS LINGUA WARB. EX DE WILD. & T.DURAND (MORACEAE) AGAINST SOME GRAM-POSITIVE AND GRAM-NEGATIVE STRAINS
10.32999/ksu2524-0838/2022-33-5
Keywords:
Ficus lingua Warb. ex De Wild. & T.Durand, Kirby-Bauer disc diffusion technique, Escherichia coli, Staphylococcus aureus, Pseudomonas aeruginosa, Enterococcus faecalis
Abstract
Many species belonging to the Ficus genus (Moraceae) contain several active compounds such as flavonoids, tannins, sesquiterpenes, alkaloids, and saponins which possess biological activities such as antioxidant, anticancer, anti-inflammation, antiviral, antibacterial, and others. In this study, we evaluated the antimicrobial activity of the ethanolic extract derived from the leaves of Ficus lingua Warb. ex De Wild. & T.Durand against some Gram-positive and Gram-negative strains in order to evaluate the possible use of this plant in preventing infections caused by these bacteria both in veterinary and medicine. The leaves of Ficus lingua, cultivated under glasshouse conditions, were sampled at M.M. Gryshko National Botanic Garden (NBG), National Academy of Science of Ukraine. The testing of the antibacterial activity of the plant extracts was carried out in vitro by the Kirby-Bauer disc diffusion technique. In the current study, Gram-negative strains such as Escherichia coli (Migula) Castellani and Chalmers (ATCC® 25922™), Escherichia coli (Migula) Castellani and Chalmers (ATCC® 35218™), Pseudomonas aeruginosa (Schroeter) Migula (ATCC® 27853™) and Gram-positive strains such as Staphylococcus aureus subsp. aureus Rosenbach (ATCC® 29213™), Staphylococcus aureus subsp. aureus Rosenbach (ATCC® 25923™), methicillin-resistant (MRSA), mecA positive Staphylococcus aureus (NCTC® 12493), Enterococcus faecalis (Andrewes and Horder) Schleifer and Kilpper-Balz (ATCC® 51299™) (resistant to vancomycin; sensitive to teicoplanin) and Enterococcus faecalis (Andrewes and Horder) Schleifer and Kilpper-Balz (ATCC® 29212™) were used. Results of the current study revealed that both Gram-positive and Gram-negative strains were sensitive to the F. lingua extract. Gram-positive strains such as S. aureus subsp. aureus Rosenbach (ATCC® 29213™), S. aureus subsp. aureus Rosenbach (ATCC® 25923™), E. faecalis (Andrewes and Horder) Schleifer and Kilpper-Balz (ATCC® 51299™) and E. faecalis (Andrewes and Horder) Schleifer and Kilpper-Balz (ATCC® 29212™) were sensitive to the F. lingua extract. The highest diameters of inhibition zones after the application of the F. lingua extract were observed for S. aureus subsp. aureus strains. This study demonstrates the antibacterial potential of ethanolic extract derived from the leaves of F. lingua and for use in the treatment of bacterial infection. The bioactive compounds of F. lingua extract, as well as its main biological activities, make it a promising candidate for communicable disease management.
References
Abdsamah O, Zaidi NT, Sule AB. Antimicrobial activity of Ficus deltoidea Jack (Mas Cotek). Pak J Pharm Sci. 2012;25(3):675-678.
African Flowering Plants Database, Conservatoire et Jardin Botaniques; Available: https://africanplantdatabase.ch/, December 17, 2022.
AlGhalban FM, Khan AA, Khattak MNK. Comparative anticancer activities of Ficus carica and Ficus salicifolia latex in MDA-MB-231 cells. Saudi J Biol Sci. 2021;28(6):3225-3234. doi:10.1016/j.sjbs.2021.02.061.
Al-Musayeib N, Ebada SS, Gad HA, Youssef FS, Ashour ML. Chemotaxonomic Diversity of Three Ficus Species: Their Discrimination Using Chemometric Analysis and Their Role in Combating Oxidative Stress. Pharmacogn Mag. 2017;13(Suppl. 3):S613-S622. doi:10.4103/pm.pm_579_16.
Aref HL, Salah KB, Chaumont JP, Fekih A, Aouni M, Said K. In vitro antimicrobial activity of four Ficus carica latex fractions against resistant human pathogens (antimicrobial activity of Ficus carica latex). Pak J Pharm Sci. 2010;23(1):53-58.
Arvaniti OS, Samaras Y, Gatidou G, Thomaidis NS, Stasinakis AS. Review on fresh and dried figs: Chemical analysis and occurrence of phytochemical compounds, antioxidant capacity and health effects. Food Res Int. 2019;119:244-267. doi:10.1016/j.foodres.2019.01.055.
Bauer AW, Kirby WM, Sherris JC, Turck M. Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol. 1966;45(4):493-496.
Berg CC, Corner EJH. Moraceae (Ficus). In: Noteboom H.P. (ed.) Flora Malesiana, Ser. 1, Vol. 17, Part 2. National Herbarium Nederland, Leiden, 2005, pp. 1-730.
Berg CC. Moreae, Artocarpeae, and Dorstenia (Moraceae), with introductions to the family and Ficus and with additions and corrections to Flora Neotropica Monograph 7. Flora Neotropica Monograph 83. The New York Botanical Garden, New York, 2001, pp. 1-346.
Clement WL, Weiblen GD. Morphological evolution in the mulberry family (Moraceae). Systematic Botany 2009;34(3):530-552.
Cook JM, Rasplus J-Y. Mutualists with attitude: coevolving fig wasps and figs. Trends in Ecology & Evolution 2003;18(5):241-248.
Cruz JMDA, Corrêa RF, Lamarão CV, et al. Ficus spp. fruits: Bioactive compounds and chemical, biological and pharmacological properties. Food Res Int. 2022;152:110928. doi:10.1016/j.foodres.2021.110928.
Cushnie TP, Lamb AJ. Antimicrobial activity of flavonoids. Int J Antimicrob Agents. 2005;26(5):343-356. doi:10.1016/j.ijantimicag.2005.09.002.
Datwyler SL, Weiblen GD. On the origin of the fig: phylogenetic relationships of Moraceae from ndhF sequences. American Journal of Botany 2004;91(5):767-777.
Deepa P, Sowndhararajan K, Kim S, Park SJ. A role of Ficus species in the management of diabetes mellitus: A review. J Ethnopharmacol. 2018;215:210-232. doi:10.1016/j.jep.2017.12.045.
Du J, Li J, Zhu J, et al. Structural characterization and immunomodulatory activity of a novel polysaccharide from Ficus carica. Food Funct. 2018;9(7):3930-3943. doi:10.1039/c8fo00603b.
El-Hawary SS, Ali ZY, Younis IY. Hepatoprotective potential of standardized Ficus species in intrahepatic cholestasis rat model: Involvement of nuclear factor-κB, and Farnesoid X receptor signaling pathways. J Ethnopharmacol. 2019;231:262-274. doi:10.1016/j.jep.2018.11.026.
Ergüden B. Phenol group of terpenoids is crucial for antibacterial activity upon ion leakage. Lett Appl Microbiol. 2021;73(4):438-445. doi:10.1111/lam.13529.
Garg VK, Paliwal SK. Wound-healing activity of ethanolic and aqueous extracts of Ficus benghalensis. J Adv Pharm Technol Res. 2011;2(2):110-114. doi:10.4103/2231-4040.82957.
Guimarães AC, Meireles LM, Lemos MF, et al. Antibacterial Activity of Terpenes and Terpenoids Present in Essential Oils. Molecules. 2019;24(13):2471. doi:10.3390/molecules24132471.
Hamed MB, El-Badry MO, Kandil EI, Borai IH, Fahmy AS. A contradictory action of procoagulant ficin by a fibrinolytic serine protease from Egyptian Ficus carica latex. Biotechnol Rep (Amst). 2020;27:e00492. doi:10.1016/j.btre.2020.e00492.
Kuete V, Kamga J, Sandjo LP, et al. Antimicrobial activities of the methanol extract, fractions and compounds from Ficus polita Vahl. (Moraceae). BMC Complement Altern Med. 2011;11:6. doi:10.1186/1472-6882-11-6.
Kuete V, Ngameni B, Simo CC, et al. Antimicrobial activity of the crude extracts and compounds from Ficus chlamydocarpa and Ficus cordata (Moraceae). J Ethnopharmacol. 2008;120(1):17-24. doi:10.1016/j.jep.2008.07.026.
Lansky EP, Paavilainen HM, Pawlus AD, Newman RA. Ficus spp. (fig): ethnobotany and potential as anticancer and anti-inflammatory agents. J Ethnopharmacol. 2008;119(2):195-213. doi:10.1016/j.jep.2008.06.025.
Lansky EP, Paavilainen HM. Figs: the genus Ficus. In: Hardman R. (ed.) Traditional herbal medicines for modern times, Vol. 9. CRC Press, Boca Raton, 2011, pp. 1-357.
Li Z, Yang Y, Liu M, et al. A comprehensive review on phytochemistry, bioactivities, toxicity studies, and clinical studies on Ficus carica Linn. leaves. Biomed Pharmacother. 2021;137:111393. doi:10.1016/j.biopha.2021.111393.
Meerungrueang W, Panichayupakaranant P. Antimicrobial activities of some Thai traditional medical longevity formulations from plants and antibacterial compounds from Ficus foveolata. Pharm Biol. 2014;52(9):1104-1109. doi:10.3109/13880209.2013.877493
Murugesu S, Selamat J, Perumal V. Phytochemistry, Pharmacological Properties, and Recent Applications of Ficus benghalensis and Ficus religiosa. Plants (Basel). 2021;10(12):2749. doi:10.3390/plants10122749.
Mutungi MM, Muema FW, Kimutai F, et al. Antioxidant and Antiproliferative Potentials of Ficus glumosa and Its Bioactive Polyphenol Metabolites. Pharmaceuticals (Basel). 2021;14(3):266. doi:10.3390/ph14030266.
Okoth DA, Chenia HY, Koorbanally NA. Antibacterial and antioxidant activities of flavonoids from Lannea alata (Engl.) Engl. (Anacardiaceae). Phytochem Lett. 2013;6:476-481. doi:10.1016/j.phytol.2013.06.003.
Pękala-Safińska A, Tkachenko H, Buyun L, Kurhaluk N, Kasiyan O, Honcharenko V, Prokopiv A, Osadowski Z. Antibacterial efficacy of leaf extract obtained from Ficus lingua Warb. ex De Wild. & T.Durand (Moraceae) against Aeromonas spp. strains. Agrobiodiversity for Improving Nutrition, Health, and Life Quality, 2019;(3):139-153. doi:10.15 414/agrobiodiversit y.2019.2585-8246.139-153.
Pinheiro PF, Menini LAP, Bernardes PC, et al. Semisynthetic Phenol Derivatives Obtained from Natural Phenols: Antimicrobial Activity and Molecular Properties. J Agric Food Chem. 2018;66(1):323-330. doi:10.1021/acs.jafc.7b04418.
Protabase – Plant Resources of Tropical Africa; Available: https://prota.prota4u.org/, December 17, 2022.
Ross JA, Kasum CM. Dietary flavonoids: bioavailability, metabolic effects, and safety. Annu Rev Nutr. 2002;22:19-34. doi:10.1146/annurev.nutr.22.111401.144957.
Silihe KK, Zingue S, Winter E, et al. Ficus umbellata Vahl. (Moraceae) Stem Bark Extracts Exert Antitumor Activities In Vitro and In Vivo. Int J Mol Sci. 2017;18(6):1073. doi:10.3390/ijms18061073.
Soni N, Dhiman RC. Larvicidal and antibacterial activity of aqueous leaf extract of Peepal (Ficus religiosa) synthesized nanoparticles. Parasite Epidemiol Control. 2020;11:e00166. doi:10.1016/j.parepi.2020.e00166
Tan Z, Deng J, Ye Q, Zhang Z. The Antibacterial Activity of Natural-derived Flavonoids. Curr Top Med Chem. 2022;22(12):1009-1019. doi:10.2174/1568026622666220221110506.
Taur DJ, Nirmal SA, Patil RY, Kharya MD. Antistress and antiallergic effects of Ficus bengalensis bark in asthma. Nat Prod Res. 2007;21(14):1266-1270. doi:10.1080/14786410701757330.
Tkachenko H, Buyun L, Osadowski Z, Honcharenko V, Prokopiv A. The antimicrobial efficacy of ethanolic extract obtained from Ficus benghalensis L. (Moraceae) leaves. Agrobiodiversity for improving nutrition, health and life quality, 2017;(1):438-445.
Tkachenko H, Buyun L, Osadowski Z, Terech-Majewska E, Honcharenko V, Prokopiv A. Comparative study of antimicrobial efficacy of the ethanolic leaf extract of Ficus benghalensis L. (Moraceae) against bacterial fish pathogens. Słupskie Prace Biologiczne, 2017;14:229-252.
Tkachenko H, Buyun L, Terech-Majewska E, Honcharenko V, Prokopiv A, Osadowski Z. Preliminary in vitro screening of the antibacterial activity of leaf extracts from various Ficus species (Moraceae) against Yersinia ruckeri. Fish. Aquat. Life, 2019;27:15-26. doi: 10.2478/aopf-2019-0002.
Tkachenko H, Buyun L, Terech-Majewska E, Osadowski Z, Sosnovskyi Y, Honcharenko V, Prokopiv A. In vitro antibacterial efficacy of various ethanolic extracts obtained from Ficus spp. leaves against the fish pathogen, Pseudomonas fluorescens. In: Globalisation and regional environment protection. The technique, technology, ecology. Eds T. Noch, W. Mikołajczewska, A. Wesołowska. Gdańsk, Gdańsk High School Publ., 2016, p. 265-286.
Tkachenko H, Buyun L, Terech-Majewska E, Osadowski Z. Antibacterial activity of ethanolic leaf extracts obtained from various Ficus species (Moraceae) against the fish pathogen. Citrobacter freundii. Baltic Coastal Zone – Journal of Ecology and Protection of the Coastline, 2016;20:117-136.
Tkachenko H, Buyun L, Terech-Majewska E, Osadowski Z. In vitro antimicrobial activity of ethanolic extracts obtained from Ficus spp. leaves against the fish pathogen Aeromonas hydrophila. Arch. Pol. Fish., 2016;24:219-230. doi: 10.1515/aopf-2016-0019.
Tkachenko HM, Buyun LI, Osadowski Z, Honcharenko VI, Prokopiv AI. Antimicrobial screening of the ethanolic leaves extract of Ficus carica L. (Moraceae) – an ancient fruit plant. Plant Introduction, 2017;1(73):78-87.
Tropical Plant Database; Available: https://ntbg.org/database/plants/, December 17, 2022.
Usman H, Abdulrahman F, Usman A. Qualitative phytochemical screening and in vitro antimicrobial effects of methanol stem bark extract of Ficus thonningii (Moraceae). Afr J Tradit Complement Altern Med. 2009;6(3):289-295. doi:10.4314/ajtcam.v6i3.57178.
Xie Y, Yang W, Tang F, Chen X, Ren L. Antibacterial activities of flavonoids: structure-activity relationship and mechanism. Curr Med Chem. 2015;22(1):132-149. doi:10.2174/0929867321666140916113443.
Yamaguchi T. Antibacterial effect of the combination of terpenoids. Arch Microbiol. 2022;204(8):520. doi:10.1007/s00203-022-03142-y.
Zar JH. Biostatistical Analysis. 4th ed., Prentice-Hall Inc., Englewood Cliffs, New Jersey,1999.
African Flowering Plants Database, Conservatoire et Jardin Botaniques; Available: https://africanplantdatabase.ch/, December 17, 2022.
AlGhalban FM, Khan AA, Khattak MNK. Comparative anticancer activities of Ficus carica and Ficus salicifolia latex in MDA-MB-231 cells. Saudi J Biol Sci. 2021;28(6):3225-3234. doi:10.1016/j.sjbs.2021.02.061.
Al-Musayeib N, Ebada SS, Gad HA, Youssef FS, Ashour ML. Chemotaxonomic Diversity of Three Ficus Species: Their Discrimination Using Chemometric Analysis and Their Role in Combating Oxidative Stress. Pharmacogn Mag. 2017;13(Suppl. 3):S613-S622. doi:10.4103/pm.pm_579_16.
Aref HL, Salah KB, Chaumont JP, Fekih A, Aouni M, Said K. In vitro antimicrobial activity of four Ficus carica latex fractions against resistant human pathogens (antimicrobial activity of Ficus carica latex). Pak J Pharm Sci. 2010;23(1):53-58.
Arvaniti OS, Samaras Y, Gatidou G, Thomaidis NS, Stasinakis AS. Review on fresh and dried figs: Chemical analysis and occurrence of phytochemical compounds, antioxidant capacity and health effects. Food Res Int. 2019;119:244-267. doi:10.1016/j.foodres.2019.01.055.
Bauer AW, Kirby WM, Sherris JC, Turck M. Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol. 1966;45(4):493-496.
Berg CC, Corner EJH. Moraceae (Ficus). In: Noteboom H.P. (ed.) Flora Malesiana, Ser. 1, Vol. 17, Part 2. National Herbarium Nederland, Leiden, 2005, pp. 1-730.
Berg CC. Moreae, Artocarpeae, and Dorstenia (Moraceae), with introductions to the family and Ficus and with additions and corrections to Flora Neotropica Monograph 7. Flora Neotropica Monograph 83. The New York Botanical Garden, New York, 2001, pp. 1-346.
Clement WL, Weiblen GD. Morphological evolution in the mulberry family (Moraceae). Systematic Botany 2009;34(3):530-552.
Cook JM, Rasplus J-Y. Mutualists with attitude: coevolving fig wasps and figs. Trends in Ecology & Evolution 2003;18(5):241-248.
Cruz JMDA, Corrêa RF, Lamarão CV, et al. Ficus spp. fruits: Bioactive compounds and chemical, biological and pharmacological properties. Food Res Int. 2022;152:110928. doi:10.1016/j.foodres.2021.110928.
Cushnie TP, Lamb AJ. Antimicrobial activity of flavonoids. Int J Antimicrob Agents. 2005;26(5):343-356. doi:10.1016/j.ijantimicag.2005.09.002.
Datwyler SL, Weiblen GD. On the origin of the fig: phylogenetic relationships of Moraceae from ndhF sequences. American Journal of Botany 2004;91(5):767-777.
Deepa P, Sowndhararajan K, Kim S, Park SJ. A role of Ficus species in the management of diabetes mellitus: A review. J Ethnopharmacol. 2018;215:210-232. doi:10.1016/j.jep.2017.12.045.
Du J, Li J, Zhu J, et al. Structural characterization and immunomodulatory activity of a novel polysaccharide from Ficus carica. Food Funct. 2018;9(7):3930-3943. doi:10.1039/c8fo00603b.
El-Hawary SS, Ali ZY, Younis IY. Hepatoprotective potential of standardized Ficus species in intrahepatic cholestasis rat model: Involvement of nuclear factor-κB, and Farnesoid X receptor signaling pathways. J Ethnopharmacol. 2019;231:262-274. doi:10.1016/j.jep.2018.11.026.
Ergüden B. Phenol group of terpenoids is crucial for antibacterial activity upon ion leakage. Lett Appl Microbiol. 2021;73(4):438-445. doi:10.1111/lam.13529.
Garg VK, Paliwal SK. Wound-healing activity of ethanolic and aqueous extracts of Ficus benghalensis. J Adv Pharm Technol Res. 2011;2(2):110-114. doi:10.4103/2231-4040.82957.
Guimarães AC, Meireles LM, Lemos MF, et al. Antibacterial Activity of Terpenes and Terpenoids Present in Essential Oils. Molecules. 2019;24(13):2471. doi:10.3390/molecules24132471.
Hamed MB, El-Badry MO, Kandil EI, Borai IH, Fahmy AS. A contradictory action of procoagulant ficin by a fibrinolytic serine protease from Egyptian Ficus carica latex. Biotechnol Rep (Amst). 2020;27:e00492. doi:10.1016/j.btre.2020.e00492.
Kuete V, Kamga J, Sandjo LP, et al. Antimicrobial activities of the methanol extract, fractions and compounds from Ficus polita Vahl. (Moraceae). BMC Complement Altern Med. 2011;11:6. doi:10.1186/1472-6882-11-6.
Kuete V, Ngameni B, Simo CC, et al. Antimicrobial activity of the crude extracts and compounds from Ficus chlamydocarpa and Ficus cordata (Moraceae). J Ethnopharmacol. 2008;120(1):17-24. doi:10.1016/j.jep.2008.07.026.
Lansky EP, Paavilainen HM, Pawlus AD, Newman RA. Ficus spp. (fig): ethnobotany and potential as anticancer and anti-inflammatory agents. J Ethnopharmacol. 2008;119(2):195-213. doi:10.1016/j.jep.2008.06.025.
Lansky EP, Paavilainen HM. Figs: the genus Ficus. In: Hardman R. (ed.) Traditional herbal medicines for modern times, Vol. 9. CRC Press, Boca Raton, 2011, pp. 1-357.
Li Z, Yang Y, Liu M, et al. A comprehensive review on phytochemistry, bioactivities, toxicity studies, and clinical studies on Ficus carica Linn. leaves. Biomed Pharmacother. 2021;137:111393. doi:10.1016/j.biopha.2021.111393.
Meerungrueang W, Panichayupakaranant P. Antimicrobial activities of some Thai traditional medical longevity formulations from plants and antibacterial compounds from Ficus foveolata. Pharm Biol. 2014;52(9):1104-1109. doi:10.3109/13880209.2013.877493
Murugesu S, Selamat J, Perumal V. Phytochemistry, Pharmacological Properties, and Recent Applications of Ficus benghalensis and Ficus religiosa. Plants (Basel). 2021;10(12):2749. doi:10.3390/plants10122749.
Mutungi MM, Muema FW, Kimutai F, et al. Antioxidant and Antiproliferative Potentials of Ficus glumosa and Its Bioactive Polyphenol Metabolites. Pharmaceuticals (Basel). 2021;14(3):266. doi:10.3390/ph14030266.
Okoth DA, Chenia HY, Koorbanally NA. Antibacterial and antioxidant activities of flavonoids from Lannea alata (Engl.) Engl. (Anacardiaceae). Phytochem Lett. 2013;6:476-481. doi:10.1016/j.phytol.2013.06.003.
Pękala-Safińska A, Tkachenko H, Buyun L, Kurhaluk N, Kasiyan O, Honcharenko V, Prokopiv A, Osadowski Z. Antibacterial efficacy of leaf extract obtained from Ficus lingua Warb. ex De Wild. & T.Durand (Moraceae) against Aeromonas spp. strains. Agrobiodiversity for Improving Nutrition, Health, and Life Quality, 2019;(3):139-153. doi:10.15 414/agrobiodiversit y.2019.2585-8246.139-153.
Pinheiro PF, Menini LAP, Bernardes PC, et al. Semisynthetic Phenol Derivatives Obtained from Natural Phenols: Antimicrobial Activity and Molecular Properties. J Agric Food Chem. 2018;66(1):323-330. doi:10.1021/acs.jafc.7b04418.
Protabase – Plant Resources of Tropical Africa; Available: https://prota.prota4u.org/, December 17, 2022.
Ross JA, Kasum CM. Dietary flavonoids: bioavailability, metabolic effects, and safety. Annu Rev Nutr. 2002;22:19-34. doi:10.1146/annurev.nutr.22.111401.144957.
Silihe KK, Zingue S, Winter E, et al. Ficus umbellata Vahl. (Moraceae) Stem Bark Extracts Exert Antitumor Activities In Vitro and In Vivo. Int J Mol Sci. 2017;18(6):1073. doi:10.3390/ijms18061073.
Soni N, Dhiman RC. Larvicidal and antibacterial activity of aqueous leaf extract of Peepal (Ficus religiosa) synthesized nanoparticles. Parasite Epidemiol Control. 2020;11:e00166. doi:10.1016/j.parepi.2020.e00166
Tan Z, Deng J, Ye Q, Zhang Z. The Antibacterial Activity of Natural-derived Flavonoids. Curr Top Med Chem. 2022;22(12):1009-1019. doi:10.2174/1568026622666220221110506.
Taur DJ, Nirmal SA, Patil RY, Kharya MD. Antistress and antiallergic effects of Ficus bengalensis bark in asthma. Nat Prod Res. 2007;21(14):1266-1270. doi:10.1080/14786410701757330.
Tkachenko H, Buyun L, Osadowski Z, Honcharenko V, Prokopiv A. The antimicrobial efficacy of ethanolic extract obtained from Ficus benghalensis L. (Moraceae) leaves. Agrobiodiversity for improving nutrition, health and life quality, 2017;(1):438-445.
Tkachenko H, Buyun L, Osadowski Z, Terech-Majewska E, Honcharenko V, Prokopiv A. Comparative study of antimicrobial efficacy of the ethanolic leaf extract of Ficus benghalensis L. (Moraceae) against bacterial fish pathogens. Słupskie Prace Biologiczne, 2017;14:229-252.
Tkachenko H, Buyun L, Terech-Majewska E, Honcharenko V, Prokopiv A, Osadowski Z. Preliminary in vitro screening of the antibacterial activity of leaf extracts from various Ficus species (Moraceae) against Yersinia ruckeri. Fish. Aquat. Life, 2019;27:15-26. doi: 10.2478/aopf-2019-0002.
Tkachenko H, Buyun L, Terech-Majewska E, Osadowski Z, Sosnovskyi Y, Honcharenko V, Prokopiv A. In vitro antibacterial efficacy of various ethanolic extracts obtained from Ficus spp. leaves against the fish pathogen, Pseudomonas fluorescens. In: Globalisation and regional environment protection. The technique, technology, ecology. Eds T. Noch, W. Mikołajczewska, A. Wesołowska. Gdańsk, Gdańsk High School Publ., 2016, p. 265-286.
Tkachenko H, Buyun L, Terech-Majewska E, Osadowski Z. Antibacterial activity of ethanolic leaf extracts obtained from various Ficus species (Moraceae) against the fish pathogen. Citrobacter freundii. Baltic Coastal Zone – Journal of Ecology and Protection of the Coastline, 2016;20:117-136.
Tkachenko H, Buyun L, Terech-Majewska E, Osadowski Z. In vitro antimicrobial activity of ethanolic extracts obtained from Ficus spp. leaves against the fish pathogen Aeromonas hydrophila. Arch. Pol. Fish., 2016;24:219-230. doi: 10.1515/aopf-2016-0019.
Tkachenko HM, Buyun LI, Osadowski Z, Honcharenko VI, Prokopiv AI. Antimicrobial screening of the ethanolic leaves extract of Ficus carica L. (Moraceae) – an ancient fruit plant. Plant Introduction, 2017;1(73):78-87.
Tropical Plant Database; Available: https://ntbg.org/database/plants/, December 17, 2022.
Usman H, Abdulrahman F, Usman A. Qualitative phytochemical screening and in vitro antimicrobial effects of methanol stem bark extract of Ficus thonningii (Moraceae). Afr J Tradit Complement Altern Med. 2009;6(3):289-295. doi:10.4314/ajtcam.v6i3.57178.
Xie Y, Yang W, Tang F, Chen X, Ren L. Antibacterial activities of flavonoids: structure-activity relationship and mechanism. Curr Med Chem. 2015;22(1):132-149. doi:10.2174/0929867321666140916113443.
Yamaguchi T. Antibacterial effect of the combination of terpenoids. Arch Microbiol. 2022;204(8):520. doi:10.1007/s00203-022-03142-y.
Zar JH. Biostatistical Analysis. 4th ed., Prentice-Hall Inc., Englewood Cliffs, New Jersey,1999.