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The Natural Products Journal

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ISSN (Print): 2210-3155
ISSN (Online): 2210-3163

Research Article

Phytochemical Study and Biological Activity of Three Fern Species of the Asplenium Genus Growing in Bulgaria

Author(s): Venelin Petkov*, Iva Slavova, Desislava Teneva, Tzvetelina Mladenova, Plamen Stoyanov and Mariana Argirova

Volume 12, Issue 6, 2022

Published on: 13 January, 2022

Article ID: e120521193308 Pages: 9

DOI: 10.2174/2210315511666210512024716

Price: $65

Abstract

Background: Ferns are underestimated as medicinal plants and their use in traditional medicine is limited despite their diversity. Most of the research on their healing properties and phytochemical composition related to their biological activity has been focused on the secondary metabolites synthesized by ferns.

Objective: In this study, we aimed to make an in-depth chemical characterization of three ferns widely spread in Bulgaria - Asplenium ceterach L., Asplenium scolopendrium L. and Asplenium trichomanes L.

Methods: Micro elemental analysis was carried out using ICP-MS. Standard laboratory methods were used to determine the content of proteins, fats and fatty acids. Chromatographic methods were applied to quantify some secondary metabolites. Two antioxidant methods and two antimicrobial tests were used to evaluate the biological properties of the ferns tested.

Results: Micro elemental analysis showed that these ferns could be useful source of zinc and iron. Protein content slightly varied among the species (13.6% - 18.4% of the dried plant weight). Negligible was the variation in oil content (3.1% - 4.0%, dry weight base); oil composition was dominated by saturated fatty acids. Some principal classes secondary metabolites, individual phenolic acids and flavonoids were quantified. The extract obtained from Asplenium ceterach L. demonstrated the highest antioxidant capacity. Fern extracts showed moderate antimicrobial activity against six of the 14 microorganisms tested.

Conclusion: The results obtained may reveal new areas of application for ferns and are a solid basis for comparison with the same species growing in other geographical and climatic conditions, which may affect their healing properties.

Keywords: Asplenium ferns, antioxidants, antimicrobial agent, microelements, fatty acids, biodiversity.

Graphical Abstract
[1]
Parihar, P.; Parihar, L. Some pteridophytes of medicinal importance from Rajasthan. Nat. Prod. Radiance, 2006, 5, 297-301.
[2]
Shakoor, A.; Anand, K.M.; Zafar, A.R.; Maheshwar, P.S. Preliminary phytochemical screening of some pteridophytes from district Shopian. Int. J. Pharm. Pharm. Sci., 2013, 5, 632-637.
[3]
Soare, L.C.; Ferdes, M.; Deliu, I.; Gibea, A. Studies regarding the antibacterial activity of some extracts of native pteridophytes, U.P.B. Sci. Bull., Series B, 2012, 74(1), 21-26.
[4]
Froissard, D.; Fons, F.; Bessière, J.M.; Buatois, B.; Rapior, S. Volatiles of French ferns and “fougère” scent in perfumery. Nat. Prod. Commun., 2011, 6(11), 1723-1726.
[http://dx.doi.org/10.1177/1934578X1100601138] [PMID: 22224297]
[5]
Petrova, A.; Vladimirov, V.; Dimitrova, D.; Ivanova, D. Proceedings of the National Workshop on Biodiversity, Sofia, BulgariaMay 2-4 20042005, pp. 75-104.954-9746-12-7
[6]
Assyov, B.; Petrova, A. Conspectus of the Bulgarian Vascular Flora: Distribution Maps and Floristic Elements, 4th ed; Bulgarian Biodiverity Foundatoin: Sofia, 2012.
[7]
Irudayaraj, V.; Johnson, M. Pharmacognostical studies on three Asplenium species. J. Phytol., 2011, 3(10), 1-9.
[8]
Živković, S.; Skorić, M.; Šiler, B.; Dmitrović, S.; Filipović, B.; Nikolić, T.; Mišić, D. Phytochemical characterization and antioxidant potential of rustyback fern (Asplenium ceterach L.). Lekovite Sirovine, 2017, 37, 15-20.
[http://dx.doi.org/10.5937/leksir1737015Z]
[9]
Mitrev, N. Health without injections (in Bulgarian). 100 medical plants; Polygraphy Publishing House: Plovdiv, 1999.
[10]
Dall’Acqua, S.; Tomè, F.; Vitalini, S.; Agradi, E.; Innocenti, G. In vitro estrogenic activity of Asplenium trichomanes L. extracts and isolated compounds. J. Ethnopharmacol., 2009, 122(3), 424-429.
[http://dx.doi.org/10.1016/j.jep.2009.02.012] [PMID: 19429306]
[11]
Stoyanov, N.; Kitanov, B. Wild beneficial plants in Bulgaria; Bulgarian Academy of Sciences: Sofia, 1960. (in Bulgarian)
[12]
Minarchenko, V.M.; Tymchenko, I.; Dvirna, T.; Makhynia, L. A review of the medicinal ferns of Ukraine. Scr. Sci. Pharm, 2017, 4(1), 7-23.
[http://dx.doi.org/10.14748/ssp.v4i1.3011]
[13]
Iwashina, T.; Matsumoto, S. Flavonoid properties of six Asplenium species in Vanuatu and New Caledonia, and distribution of flavonoid and related compounds in Asplenium. Bull. Natl. Mus. Nat. Sci. Ser. B, 2011, 37(3), 133-145.
[14]
Berk, S.; Tepe, B.; Arslan, S.; Sarikurkcu, C. Screening of the antioxidant, antimicrobial and DNA damage protection potentials of the aqueous extract of Asplenium ceterach DC. Afr. J. Biotechnol., 2011, 10(44), 8902-8908.
[15]
Bahadori, M.B.; Mahmoodi Kordi, F.; Ahmadi, A.A.; Bahadori, Sh.; Valizade, H. Antibacterial evaluation and preliminary phytochemical screening of selected ferns from Iran. Res. J. Pharmacogn, 2015, 2(2), 53-59.
[16]
Valizadeh, H.; Sonboli, A.; Kordi, F.M.; Dehghan, H.; Bahadori, M.B. Cytotoxicity, antioxidant activity and phenolic content of eight fern species, from north of Iran. Pharm. Sci., 2016, 21(1), 18-24.
[http://dx.doi.org/10.15171/PS.2015.12]
[17]
Jarial, R.; Thakur, S.; Sakinah, M.; Zularisam, A.W.; Sharad, A.; Kanwar, S.S.; Singh, L. Potent anticancer, antioxidant and antibacterial activities of isolated flavonoids from Asplenium nidus. J. King Saud Univ. Sci., 2018, 30(2), 185-192.
[http://dx.doi.org/10.1016/j.jksus.2016.11.006]
[18]
Liu, Y.; Wujisguleng, W.; Long, C. Food uses of ferns in China: a review. Acta Soc. Bot. Pol., 2012, 81(4), 263-270.
[http://dx.doi.org/10.5586/asbp.2012.046]
[19]
American Oil Chemists Society (AOAC). Kjeldahl’s method for protein determination in cereals and feed. In: Official Methods of Analysis℠, 16th ed.; AOAC International, 1996.
[20]
International Organization for Standardization (ISO Standard No. 659:2009). Oilseeds – Determination of oil content (Reference method), 2009.
[21]
International Organization for Standardization (ISO Standard No. 5509:2000). Animal and vegetable fats and oils – Preparation of methyl esters of fatty acids, 2000.
[22]
International Organization for Standardization (ISO Standard No. 5508:2004). Animal and vegetable fats and oils. Analysis by gas chromatography of methyl esters of fatty acids, 2004.
[23]
Morado-Castillo, R.; Quintanilla-Licea, R.; Gomez-Flores, R.; Blaschek, W. Total phenolic and flavonoid contents and flavonoid composition of flowers and leaves from the Mexican medicinal plant Gymno spermaglutinosum (Spreng.) Less’. European J. Med. Plants, 2016, 15(4), 1-8.
[http://dx.doi.org/10.9734/EJMP/2016/28028]
[24]
Hagerman, A.E.; Butler, L.G. Protein precipitation method for the quantitative determination of tannins. J. Agric. Food Chem., 1978, 26(4), 809-812.
[http://dx.doi.org/10.1021/jf60218a027]
[25]
Haldar, D.; Sen, D.; Gayen, K. Development of spectrophotometric method for the analysis of multi-component carbohydrate mixture of different moieties. Appl. Biochem. Biotechnol., 2017, 181(4), 1416-1434.
[http://dx.doi.org/10.1007/s12010-016-2293-3] [PMID: 27787768]
[26]
Ivanov, I.G.; Vrancheva, R.Z.; Marchev, A.S.; Petkova, N.T.; Aneva, I.Y.; Denev, P.P.; Georgiev, V.G.; Pavlov, A.I. Antioxidant activities and phenolic compounds in Bulgarian Fumaria species. Int. J. Curr. Microbiol. Appl. Sci., 2014, 3(2), 296-306.
[27]
Serpen, A.; Capuano, E.; Fogliano, V.; Gökmen, V. A new procedure to measure the antioxidant activity of insoluble food components. J. Agric. Food Chem., 2007, 55(19), 7676-7681.
[http://dx.doi.org/10.1021/jf071291z] [PMID: 17708649]
[28]
Berker, K.I.; Güçlü, K.; Demirata, B.; Apak, R. A novel antioxidant assay of ferric reducing capacity measurement using ferrozine as the colour forming complexation reagent. Anal. Methods-UK, 2010, 2, 1770-1778.
[29]
Jirovetz, L.; Buchbauer, G.; Denkova, Z.; Slavchev, A.; Stoyanova, A.; Schmidt, E. Chemical composition, antimicrobial activities and odor descriptions of various Salvia sp. and Thuja sp. essential oils. Ernahrung/Nutrition, 2006, 30, 152-159.
[30]
Cindrić, I.J.; Zeiner, M.; Glamuzina, E.; Stingeder, G. Elemental characterisation of the medical herbs Salvia officinalis L. and Teucrium montanum L. grown in Croatia. Microchem. J., 2013, 107, 185-189.
[http://dx.doi.org/10.1016/j.microc.2012.06.013]
[31]
Pytlakowska, K.; Kita, A.; Janoska, P.; Połowniak, M.; Kozik, V. Multi-element analysis of mineral and trace elements in medicinal herbs and their infusions. Food Chem., 2012, 135(2), 494-501.
[http://dx.doi.org/10.1016/j.foodchem.2012.05.002] [PMID: 22868119]
[32]
Colombo, C.; Palumbo, G.; He, J-Z.; Pinton, R.; Cesco, S. Review on iron availability in soil: interaction of Fe minerals, plants, and microbes. J. Soils Sediments, 2014, 14, 538-548.
[http://dx.doi.org/10.1007/s11368-013-0814-z]
[33]
Greeshma, A.A.; Sridhar, K.R. Nutraceutical and bioactive significance of ferns with emphasis on the medicinal fern diplazium.Medically Important Plant Biomes: Source of Secondary Metabolites. Microorganisms for Sustainability; Egamberdieva, D.; Tiezzi, A., Eds.; Springer: Singapore, 2019, Vol. 15, pp. 115-131.
[http://dx.doi.org/10.1007/978-981-13-9566-6_6]
[34]
Nekrasov, E.V.; Svetashev, V.I.; Khrapko, O.V.; Vyssotski, M.V. Variability of fatty acid profiles in ferns: Relation to fern taxonomy and seasonal development. Phytochemistry, 2019, 162, 47-55.
[http://dx.doi.org/10.1016/j.phytochem.2019.02.015] [PMID: 30856529]
[35]
Salehzadeh, A.; Naeemi, A.S.; Arasteh, A. Biodiesel Production from Azolla filiculoides (Water Fern). Trop. J. Pharm. Res., 2014, 13(6), 957-960.
[http://dx.doi.org/10.4314/tjpr.v13i6.19]
[36]
Redel-Macías, M.D.; Pinzi, S.; Ruz, M.F.; Cubero-Atienza, A.J.; Dorado, M.P. Biodiesel from saturated and monounsaturated fatty acid methyl esters and their influence over noise and air pollution. Fuel, 2012, 97, 751-756.
[http://dx.doi.org/10.1016/j.fuel.2012.01.070]
[37]
Sierra-Cantor, J.F.; Guerrero-Fajardo, C.A. Methods for improving the cold flow properties of biodiesel with high saturated fatty acids content: A review. Renew. Sustain. Energy Rev., 2017, 72, 774-790.
[http://dx.doi.org/10.1016/j.rser.2017.01.077]
[38]
Lai, H.Y.; Lim, Y.Y. Antioxidant properties of some Malaysian ferns. 3rd International Conference on Chemical, Biological and Environmental Engineering (IPCBEE), Chengdu, ChinaSeptember 23-25,2011, Vol. 20, pp. 8-12.
[39]
Kazazic, M. Djapo; Ademovic, E. Antioxidant activity of water extracts of some medicinal plants from Herzegovina region. Int. J. Pure App. Biosci, 2016, 4(2), 85-90.
[http://dx.doi.org/10.18782/2320-7051.2251]
[40]
Doshi, G.M.; Nalawade, V.V.; Mukadam, A.S.; Chaskar, P.K.; Zine, S.P.; Somani, R.R.; Une, H.D. Elucidation of flavonoids from Carissa congesta, Polyalthia longifolia, and Benincasa hispida plant extracts by hyphenated technique of liquid chromatography-mass spectroscopy. Pharmacognosy Res., 2016, 8(4), 281-286.
[http://dx.doi.org/10.4103/0974-8490.186578] [PMID: 27695269]
[41]
Xiao, J. Dietary flavonoid aglycones and their glycosides: Which show better biological significance? Crit. Rev. Food Sci. Nutr., 2017, 57(9), 1874-1905.
[PMID: 26176651]
[42]
Lee, C.H.; Shin, S.L. Functional activities of ferns for human health.Working with Ferns: Issues and Applications; Fernández, H.; Kumar, A.; Revilla, A., Eds.; Springer: New York, 2010, pp. 347-359.
[43]
Tzanova, M.T.; Grozeva, N.H.; Gerdzhikova, M.A.; Argirova, M.D.; Pavlov, D.H.; Terzieva, S.R. Flavonoid content and antioxidant activity of Betonica bulgarica Degen et Neič’. Izv. Him., 2018, 50, 90-97.
[44]
Tomova, T.; Petkov, V.; Slavova, I.; Stoyanov, P.; Argirova, M. Naturally present metal ions in plants could interfere with common antioxidant assays. MethodsX, 2020, 7100995
[http://dx.doi.org/10.1016/j.mex.2020.100995] [PMID: 32760660]
[45]
Xie, J.; Schaich, K.M. Re-evaluation of the 2,2-diphenyl-1-picrylhydrazyl free radical (DPPH) assay for antioxidant activity. J. Agric. Food Chem., 2014, 62(19), 4251-4260.
[http://dx.doi.org/10.1021/jf500180u] [PMID: 24738928]
[46]
MacDonald‐Wicks, L.K.; Wood, L.G.; Garg, M.L. Methodology for the determination of biological antioxidant capacity in vitro: A review. J. Sci. Food Agric., 2006, 86(13), 2046-2056.
[http://dx.doi.org/10.1002/jsfa.2603]
[47]
Chew, Y.L.; Goh, J.K.; Lim, Y.Y. Assessment of in vitro antioxidant capacity and polyphenolic composition of selected medicinal herbs from Leguminosae family in Peninsular Malaysia. Food Chem., 2009, 116, 13-18.
[http://dx.doi.org/10.1016/j.foodchem.2009.01.091]
[48]
Lai, H.Y.; Lim, Y.Y.; Tan, S.P. Antioxidative, tyrosinase inhibiting and antibacterial activities of leaf extracts from medicinal ferns. Biosci. Biotechnol. Biochem., 2009, 73(6), 1362-1366.
[http://dx.doi.org/10.1271/bbb.90018] [PMID: 19502733]
[49]
Delcour, A.H. Outer membrane permeability and antibiotic resistance. Biochim. Biophys. Acta, 2009, 1794(5), 808-816.
[http://dx.doi.org/10.1016/j.bbapap.2008.11.005] [PMID: 19100346]
[50]
Sahayaraj, K.; Francis Borgio, J.A.; Raju, G. Antifungal activity of three fern extracts on causative agents of groundnut early leaf spot and rust diseases. J. Plant Prot. Res., 2009, 49(2), 142-144.
[http://dx.doi.org/10.2478/v10045-009-0019-z]
[51]
Singh, H.B. Potential medicinal Pteridophytes of India and other chemical constituents. J. Econ. Taxon. Bot., 1999, 23(1), 63-78.
[52]
Živković, S.; Milutinović, M.; Maksimović, V.; Ćirić, A.; Ivanov, M.; Božunović, J.; Banjanac, T.; Mišić, D. Antioxidant and antimicrobial activity of two Asplenium species. S. Afr. J. Bot., 2020, 132, 180-187.
[http://dx.doi.org/10.1016/j.sajb.2020.03.034]
[53]
World Health Organization (WHO). Antimicrobial resistance, Available at: https://www.who.int/news-room/fact-sheets/detail/antimicrobial-resistance Accessed November 06, 2020
[54]
Diniz-Silva, H.T.; Magnani, M.; Siqueira, S.; Souza, E.L.; Siqueira-Júnior, J.P. Fruit flavonoids as modulators of norfloxacin resistance in Staphylococcus aureus that overexpresses norA’ LWT – Food Sci. Technol, 2017, 85(B), 324-326.
[55]
Cao, H.; Chai, T.T.; Wang, X.; Morais-Braga, M.F.B.; Yang, J.H.; Wong, F.C.; Wang, R.; Yao, H.; Cao, J.; Cornara, L.; Burlando, B.; Wang, Y.; Xiao, J.; Coutinho, H.D.M. Phytochemicals from fern species: potential for medicine applications. Phytochem. Rev., 2017, 16(3), 379-440.
[http://dx.doi.org/10.1007/s11101-016-9488-7] [PMID: 32214919]

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