The phenolic composition, as well as the antioxidant and antimicrobial activities of two poorly investigated Achillea species, Achillea lingulata Waldst. and the endemic Achillea abrotanoides Vis., were studied. To obtain a more detailed phytochemical profile, four solvents with different polarities were used for the preparation of the plant extracts whose phenolic composition was analyzed using UHPLC-MS/MS (ultra-high performance liquid chromatography-tandem mass spectrometry). The results indicate that both of the investigated Achillea species are very rich in both phenolic acids and flavonoids, but that their profiles differ significantly. Chloroform extracts from both species had the highest yields and were the most chemically versatile. The majority of the examined extracts showed antimicrobial activity, while ethanolic extracts from both species were potent against all tested microorganisms. Furthermore, the antioxidant activity of the extracts was evaluated. It was found that the ethanolic extracts possessed the strongest antioxidant activities, although these extracts did not contain the highest amounts of detected phenolic compounds. In addition, several representatives of phenolic compounds were also assayed for these biological activities. Results suggest that ethanol is a sufficient solvent for the isolation of biologically active compounds from both Achillea species. Moreover, it was shown that the flavonoids naringenin and morin are mainly responsible for these antimicrobial activities, while caffeic, salicylic, chlorogenic, p-coumaric, p-hydroxybenzoic, and rosmarinic acid are responsible for the antioxidant activities of the Achillea extracts.

Centre of Region Haná for Biotechnological and Agricultural Research Palacky University Šlechtitelů 27 78371 Olomouc Czech Republic

Centre of the Region Haná for Biotechnological and Agricultural Research Department of Genetic Resources for Vegetables Medicinal and Special Plants Crop Research Institute Šlechtitelů 29 78371 Olomouc Czech Republic

Laboratory for Microbiology Department of Biology Faculty of Science University of Sarajevo Zmaja od Bosne 33 35 71 000 Sarajevo Bosnia and Herzegovina

Laboratory for Plant Physiology Department of Biology Faculty of Science University of Sarajevo Zmaja od Bosne 33 35 71 000 Sarajevo Bosnia and Herzegovina

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Grodowska K., Parczewski A. Organic solvents in the pharmaceutical industry. Acta Pol. Pharm. Drug Res. 2010;67:3–12. PubMed

González-Montelongo R., Lobo M.G., González M. Antioxidant activity in banana peel extracts: Testing extraction conditions and related bioactive compounds. Food Chem. 2010;119:1030–1039. doi: 10.1016/j.foodchem.2009.08.012. DOI

Dorta E., Lobo M.G., Gonzalez M. Reutilization of mango byproducts: Study of the effect of extraction solvent and temper-ature on their antioxidant properties. J. Food Sci. 2012;77:80–88. doi: 10.1111/j.1750-3841.2011.02477.x. PubMed DOI

Lafka T.-I., Sinanoglou V., Lazos E.S. On the extraction and antioxidant activity of phenolic compounds from winery wastes. Food Chem. 2007;104:1206–1214. doi: 10.1016/j.foodchem.2007.01.068. DOI

Lapkin A.A., Plucinski P.K., Cutler M. Comparative Assessment of Technologies for Extraction of Artemisinin. J. Nat. Prod. 2006;69:1653–1664. doi: 10.1021/np060375j. PubMed DOI

Tyśkiewicz K., Konkol M., Rój E. The Application of supercritical fluid extraction in phenolic compounds isolation from natural plant materials. Molecules. 2018;23:2625. doi: 10.3390/molecules23102625. PubMed DOI PMC

Essien S.O., Young B., Baroutian S. Recent advances in subcritical water and supercritical carbon dioxide extraction of bioactive compounds from plant materials. Trends Food Sci. Technol. 2020;97:156–169. doi: 10.1016/j.tifs.2020.01.014. DOI

Villanueva-Bermejo D., Zahran F., Troconis D., Villalva M., Reglero G., Fornari T. Selective precipitation of phenolic compounds from Achillea millefolium L. extracts by supercritical anti-solvent technique. J. Supercrit. Fluids. 2017;120:52–58. doi: 10.1016/j.supflu.2016.10.011. DOI

Chemat F., Rombaut N., Sicaire A.-G., Meullemiestre A., Fabiano-Tixier A.-S., Abert-Vian M. Ultrasound assisted extraction of food and natural products. Mechanisms, techniques, combinations, protocols and applications. A review. Ultrason. Sonochemistry. 2017;34:540–560. doi: 10.1016/j.ultsonch.2016.06.035. PubMed DOI

Savic Gajic I., Savic I., Boskov I., Žerajić S., Markovic I., Gajic D. Optimization of ultrasound-assisted extraction of phenolic compounds from black locust (Robiniae Pseudoacaciae) flowers and comparison with conventional methods. Antioxidants. 2019;8:248. doi: 10.3390/antiox8080248. PubMed DOI PMC

Savic I.M., Gajic I.M.S. Optimization of ultrasound-assisted extraction of polyphenols from wheatgrass (Triticum aestivum L.) J. Food Sci. Technol. 2020;57:2809–2818. doi: 10.1007/s13197-020-04312-w. PubMed DOI PMC

Paswan R., Park Y.W. Survivability of Salmonella and Escherichia coli O157:H7 pathogens and food safety concerns on com-mercial powder milk products. Dairy. 2020;1:189–201. doi: 10.3390/dairy1030014. DOI

Syahrul F., Wahyuni C.U., Notobroto H.B., Wasito E.B., Adi A.C., Dwirahmadi F. Transmission media of foodborne diseases as an index prediction of diarrheagenic Escherichia coli: Study at elementary school, Surabaya, Indonesia. Int. J. Environ. Res. Pub. Health. 2020;17:8227. doi: 10.3390/ijerph17218227. PubMed DOI PMC

Abril A.G., Villa T.G., Barros-Velázquez J., Cañas B., Sánchez-Pérez A., Calo-Mata P., Carrera M. Staphylococcus aureus Exotoxins and Their Detection in the Dairy Industry and Mastitis. Toxins. 2020;12:537. doi: 10.3390/toxins12090537. PubMed DOI PMC

Higaki S., Kitagawa T., Kagoura M., Morohashi M., Yamagishi T. Predominant Staphylococcus aureus isolated from various skin diseases. J. Int. Med Res. 2000;28:187–190. doi: 10.1177/147323000002800404. PubMed DOI

Principi N., Argentiero A., Neglia C., Gramegna A., Esposito S. New antibiotics for the treatment of acute bacterial skin and soft tissue infections in pediatrics. Pharmaceuticals. 2020;13:333. doi: 10.3390/ph13110333. PubMed DOI PMC

Appelbaum P.C. Microbiology of antibiotic resistance in Staphylococcus aureus. Clin. Infect. Dis. 2007;45:S165–S170. doi: 10.1086/519474. PubMed DOI

Gregova G., Kmetova M., Kmet V., Venglovsky J., Feher A. Antibiotic resistance of Escherichia coli isolated from a poultry slaughterhouse. Ann. Agric. Environ. Med. 2012;19:75–77. PubMed

Darwish R.M., Aburjai T.A. Effect of ethnomedicinal plants used in folklore medicine in Jordan as antibiotic resistant in-hibitors on Escherichia coli. BMC Compl. Alternative Med. 2010;10:1–8. doi: 10.1186/1472-6882-10-9. PubMed DOI PMC

Nyakudya T., Tshabalala T., Dangarembizi R., Erlwanger K., Ndhlala A.R. The potential therapeutic value of medicinal plants in the management of metabolic disorders. Molecules. 2020;25:2669. doi: 10.3390/molecules25112669. PubMed DOI PMC

Akinyede K.A., Ekpo O.E., Oguntibeju O.O. Ethnopharmacology, therapeutic properties and nutritional potentials of Car-pobrotus edulis: A comprehensive review. Sci. Pharm. 2020;88:39. doi: 10.3390/scipharm88030039. DOI

Tavares W.R., Barreto M.D.C., Seca A.M.L. Uncharted source of medicinal products: The case of the Hedychium genus. Medicines. 2020;7:23. doi: 10.3390/medicines7050023. PubMed DOI PMC

Altemimi A., Lakhssassi N., Baharlouei A., Watson D.G., Lightfoot D.A. Phytochemicals: Extraction, isolation, and iden-tification of bioactive compounds from plant extracts. Plants. 2017;6:42. doi: 10.3390/plants6040042. PubMed DOI PMC

Kostić A.Ž., Janaćković P., Kolašinac S.M., Stevanović Z.P.D. Balkans’ Asteraceae species as a source of biologically active compounds for the pharmaceutical and food industry. Chem. Biodivers. 2020;17:2000097. doi: 10.1002/cbdv.202000097. PubMed DOI

Bessada S.M., Barreira J.C., Oliveira M.P. Asteraceae species with most prominent bioactivity and their potential applications: A review. Ind. Crop. Prod. 2015;76:604–615. doi: 10.1016/j.indcrop.2015.07.073. DOI

Michel J., Rani N.Z.A., Husain K. A review on the potential use of medicinal plants from Asteraceae and Lamiaceae plant family in cardiovascular diseases. Front. Pharmacol. 2020;11:852. doi: 10.3389/fphar.2020.00852. PubMed DOI PMC

Ross J. Combining Western Herbs and Chinese Medicine: Principles, Practice, and Materia Medica. Greenfields press; Seattle, WA, USA: 2003. pp. 165–182.

Saeidnia S., Gohari A., Mokhber-Dezfuli N., Kiuchi F. A review on phytochemistry and medicinal properties of the genus Achillea. DARU J. Pharm. Sci. 2011;19:173–186. PubMed PMC

Radulovic N., Zlatković B., Palic R., Stojanovic G. Chemotaxonomic significance of the Balkan Achillea volatiles. Nat. Prod. Commun. 2007;2:453–474. doi: 10.1177/1934578X0700200417. DOI

Boskovic Z., Radulovic N., Stojanovic G. Essential oil composition of four Achillea species from the Balkans and its chemo-taxonomic significance. Chem. Nat. Compd. 2005;41:674–678. doi: 10.1007/s10600-006-0009-6. DOI

G.rada Publishing . Pharmacopoea Bohemica MMXVII. 1st ed. G.rada Publishing; Prague, Czech Republic: 2017. p. 4121.

Jovanović O., Radulović N., Palić R., Zlatković B. Root essential oil of Achillea lingulata Waldst. & Kit. (Asteraceae) J. Essent. Oil Res. 2010;22:336–339. doi: 10.1080/10412905.2010.9700340. DOI

Stojanovic G., Hashimoto T., Asakawa Y., Palić R. Chemical composition of the Achillea lingulata extract. Biochem. Syst. Ecol. 2005;33:207–210. doi: 10.1016/j.bse.2004.07.004. DOI

Zhang Q.W., Lin L.G., Ye W.C. Techniques for extraction and isolation of natural products: A comprehensive review. Chin. Med. 2018;13:1–26. doi: 10.1186/s13020-018-0177-x. PubMed DOI PMC

Truong D.-H., Nguyen D.H., Ta N.T.A., Bui A.V., Do T.H., Nguyen H.C. Evaluation of the use of different solvents for phytochemical constituents, antioxidants, and in vitro anti-inflammatory activities of Severinia buxifolia. J. Food Qual. 2019;2019:1–9. doi: 10.1155/2019/8178294. DOI

Trifunović S., Vajs V., Tešević V., Djoković D., Milosavljević S. Lignans from the plant species Achillea lingulata. J. Serbian Chem. Soc. 2003;68:277–280. doi: 10.2298/JSC0305277T. DOI

Chalchat J.C., Gorunovic M.S., Petrovic S.D., Zlatkovic V.V. Aromatic plants of Yugoslavia. II. Chemical composition of essential oils of three wild Achillea Species: A. clavenae L., A. collina Becker and A. lingulata W. et K. J. Essent. Oil Res. 2000;12:7–10. doi: 10.1080/10412905.2000.9712028. DOI

Stojanovic G., Palic R., Naskovic T., Dokovic D., Milosavljevic S. Volatile constituents of Achillea lingulata WK. J. Essent. Oil Res. 2001;13:378–379. doi: 10.1080/10412905.2001.9712239. DOI

Kovačević N.N., Ristić M.S., Tasić S.R., Menković N.R., Grubišić D.V., Đoković D.D. Comparative study of essential oil of three Achillea species from Serbia. J. Essent. Oil Res. 2005;17:57–60. doi: 10.1080/10412905.2005.9698830. DOI

Kundakovic T., Fokialakis N., Kovacevic N., Chinou I. Essential oil composition of Achillea lingulata and A. umbellata. Flavour Fragr. J. 2007;22:184–187. doi: 10.1002/ffj.1778. DOI

Popovici M., Vlase L., Oniga I., Tamas M. HPLC analyses on polyphenolic compounds from Achillea species. Farmacia. 2007;3:353–357.

Serdar G., Sökmen M., Demir E., Sökmen A., Bektaş E. Extraction of antioxidative principles of Achillea biserrata M. Bieb. and chromatographic analyses. Int. J. Second. Metab. 2015;2:3–15. doi: 10.21448/ijsm.240706. DOI

Bashi D.S., Mortazavi S.A., Rezaei K., Rajaei A., Karimkhani M.M. Optimization of ultrasound-assisted extraction of phenolic compounds from yarrow (Achillea beibrestinii) by response surface methodology. Food Sci. Biotechnol. 2012;21:1005–1011. doi: 10.1007/s10068-012-0131-0. DOI

Benedec D., Vlase L., Oniga I., Mot A.C., Damian G., Hanganu D., Duma M., Silaghi-Dumitrescu R. Polyphenolic composition, antioxidant and antibacterial activities for two Romanian subspecies of Achillea distans Waldst. et Kit. ex Willd. Molecules. 2013;18:8725–8739. doi: 10.3390/molecules18088725. PubMed DOI PMC

Tuberoso C.I.G., Montoro P., Piacente S., Corona G., Deiana M., Dessì M.A., Pizza C., Cabras P. Flavonoid characterization and antioxidant activity of hydroalcoholic extracts from Achillea ligustica All. J. Pharm. Biomed. Anal. 2009;50:440–448. doi: 10.1016/j.jpba.2009.05.032. PubMed DOI

Karlova K. Accumulation of flavonoid compounds in flowering shoots of Achillea colllina Becker ex. Rchb. Alba during flower development. Hortic. Sci. 2006;33:158–162. doi: 10.17221/3756-HORTSCI. DOI

Lemmens-Gruber R., Marchart E., Rawnduzi P., Engel N., Benedek B., Kopp B. Investigation of the spasmolytic activity of the flavonoid fraction of Achillea millefolium s.l. on isolated Guinea-pig ilea. Arzneimittelforschung. 2006;56:582–588. doi: 10.1055/s-0031-1296755. PubMed DOI

Benedec D., Hanganu D., Oniga I., Filip L., Bischin C., Silaghi-Dumitrescu R., Tiperciuc B., Vlase L. Achillea schurii Flowers: Chemical, antioxidant, and antimicrobial investigations. Molecules. 2016;21:1050. doi: 10.3390/molecules21081050. PubMed DOI PMC

Stojanović G., Radulović N., Hashimoto T., Palić R. In vitro antimicrobial activity of extracts of four Achillea species: The composition of Achillea clavennae L. (Asteraceae) extract. J. Ethnopharmacol. 2005;101:185–190. doi: 10.1016/j.jep.2005.04.026. PubMed DOI

Candan F., Unlu M., Tepe B., Daferera D., Polissiou M., Sökmen A., Akpulat H. Antioxidant and antimicrobial activity of the essential oil and methanol extracts of Achillea millefolium subsp. millefolium Afan. (Asteraceae). J. Ethnopharmacol. 2003;87:215–220. doi: 10.1016/S0378-8741(03)00149-1. PubMed DOI

Mudzengi C.P., Murwira A., Tivapasi M., Murungweni C., Burumu J.V., Halimani T. Antibacterial activity of aqueous and methanol extracts of selected species used in livestock health management. Pharm. Biol. 2017;55:1054–1060. doi: 10.1080/13880209.2017.1287744. PubMed DOI PMC

Gonelimali F.D., Lin J., Miao W., Xuan J., Charles F., Chen M., Hatab S.R. Antimicrobial properties and mechanism of action of some plant extracts against food pathogens and spoilage microorganisms. Front. Microbiol. 2018;9:1639. doi: 10.3389/fmicb.2018.01639. PubMed DOI PMC

Maz M., Mirdeilami S.Z., Pessarakli M. Essential oil composition and antibacterial activity of Achillea millefolium L. from different regions in North east of Iran. J. Med. Plant Res. 2013;7:1063–1069. doi: 10.5897/JMPR12.961. DOI

Bouarab-Chibane L., Forquet V., Lantéri P., Clément Y., Léonard-Akkari L., Oulahal N., Degraeve P., Bordes C. Anti-bacterial properties of polyphenols: Characterization and QSAR (Quantitative structure–activity relationship) models. Front. Microbiol. 2019;10:829. doi: 10.3389/fmicb.2019.00829. PubMed DOI PMC

Ikigai H., Nakae T., Hara Y., Shimamura T. Bactericidal catechins damage the lipid bilayer. Biochim. et Biophys. Acta (BBA) Biomembr. 1993;1147:132–136. doi: 10.1016/0005-2736(93)90323-R. PubMed DOI

Taguri T., Tanaka T., Kouno I. Antibacterial spectrum of plant polyphenols and extracts depending upon hydroxyphenyl structure. Biol. Pharm. Bull. 2006;29:2226–2235. doi: 10.1248/bpb.29.2226. PubMed DOI

Cushnie T.T., Lamb A.J. Recent advances in understanding the antibacterial properties of flavonoids. Int. J. Antimicrob. Agents. 2011;38:99–107. doi: 10.1016/j.ijantimicag.2011.02.014. PubMed DOI

Borges A., Ferreira C., Saavedra M.J., Simões M. Antibacterial activity and mode of action of ferulic and gallic acids against pathogenic bacteria. Microb. Drug Resist. 2013;19:256–265. doi: 10.1089/mdr.2012.0244. PubMed DOI

Tsuchiya H., Sato M., Miyazaki T., Fujiwara S., Tanigaki S., Ohyama M., Tanaka T., Iinuma M. Comparative study on the antibacterial activity of phytochemical flavanones against methicillin-resistant Staphylococcus aureus. J. Ethnopharmacol. 1996;50:27–34. doi: 10.1016/0378-8741(96)85514-0. PubMed DOI

Barchan A., Bakkali M., Arakrak A., Pagán R., Laglaoui A. The effects of solvents polarity on the phenolic contents and antioxidant activity of three Mentha species extracts. Int. J. Curr. Microbiol. Appl. Sci. 2014;3:399–412.

Anwar F., Przybylski R. Effect of solvents extraction on total phenolics and antioxidant activity of extracts from flaxseed (Linum usitatissimum L.) Acta Sci. Pol. Technol. Aliment. 2012;11:293–302. PubMed

Lanfer-Marquez U.M., Barros R.M., Sinnecker P. Antioxidant activity of chlorophylls and their derivatives. Food Res. Int. 2005;38:885–891. doi: 10.1016/j.foodres.2005.02.012. DOI

Gaweł-Bęben K., Strzępek-Gomółka M., Czop M., Sakipova Z., Głowniak K., Kukula-Koch W. Achillea millefolium L. and Achillea biebersteinii Afan. hydroglycolic extracts–bioactive ingredients for cosmetic use. Molecules. 2020;25:3368. doi: 10.3390/molecules25153368. PubMed DOI PMC

Bozin B., Mimica-Dukic N., Bogavac M., Suvajdzic L., Simin N., Samojlik I., Couladis M. Chemical composition, antiox-idant and antibacterial properties of Achillea collina Becker ex Heimerl s.l. and A. pannonica scheele essential oils. Molecules. 2008;13:2058–2068. doi: 10.3390/molecules13092058. PubMed DOI PMC

Gharibi S., Tabatabaei B.E.S., Saeidi G. Comparison of essential oil composition, flavonoid content and antioxidant activity in eight Achillea species. J. Essent. Oil Bear. Plants. 2015;18:1382–1394. doi: 10.1080/0972060X.2014.981600. DOI

Kazemi M. Chemical composition and antimicrobial, antioxidant activities and anti-inflammatory potential of Achillea mille-folium L., Anethum graveolens L., and Carum copticum L. essential oils. J. Herb. Med. 2015;5:217–222. doi: 10.1016/j.hermed.2015.09.001. DOI

Milutinovic M., Radovanovic N., Corovic M., Siler-Marinkovic S., Rajilic-Stojanovic M., Dimitrijevic-Brankovic S. Opti-misation of microwave-assisted extraction parameters for antioxidants from waste Achillea millefolium dust. Ind. Crop Prod. 2015;77:333–341. doi: 10.1016/j.indcrop.2015.09.007. DOI

Venditti A., Maggi F., Vittori S., Papa F., Serrilli A.M., Di Cecco M., Ciaschetti G., Mandrone M., Poli F., Bianco A. Antioxidant andα-glucosidase inhibitory activities of Achillea tenorii. Pharm. Biol. 2015;53:1505–1510. doi: 10.3109/13880209.2014.991833. PubMed DOI

Meda A., Lamien C.E., Romito M., Millogo J., Nacoulma O.G. Determination of the total phenolic, flavonoid and proline contents in Burkina Fasan honey, as well as their radical scavenging activity. Food Chem. 2005;91:571–577. doi: 10.1016/j.foodchem.2004.10.006. DOI

Valgas C., De Souza S.M., Smania E.F.A., Smania A., Jr. Screening methods to determine antibacterial activity of natural products. Braz. J. Microbiol. 2007;38:369–380. doi: 10.1590/S1517-83822007000200034. DOI

Magaldi S., Mata-Essayag S., de Capriles C.H., Perez C., Colella M., Olaizola C., Ontiveros Y. Well diffusion for antifungal susceptibility testing. Int. J. Infect. Dis. 2004;8:39–45. doi: 10.1016/j.ijid.2003.03.002. PubMed DOI

McFarland J. The nephelometer: An instrument for estimating the number of bacteria in suspensions used for calculating the opsonic index and for vaccines. JAMA. 1907;XLIX:1176–1178. doi: 10.1001/jama.1907.25320140022001f. DOI