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Comparative analysis of antioxidant, antimicrobiological and cytotoxic activities of native and fermented chamomile ligulate flower extracts

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The work investigated differences in apigenin content, as well as in other compounds, and examined the chemical profiles, antioxidant, antimicrobial and cytotoxic effects of extracts obtained from native and fermented chamomile ligulate flowers.

Chamomile (Chamomilla recutita L.) has a long history of being used as a medicinal plant due to many health benefits, including antiinflammatory, anticancer, antispasmodic, radical-scavenging effects and others. Apigenin is recognized as one of the most bioactive phenolic compounds in chamomile. In comparison to its bound forms, which include mostly apigenin-7-O-β-glucoside and various acylated forms, the aglycone is attributed with much higher bioactivity. Due to this fact, in this work ligulate florets of chamomile anthodium were subjected to a fermentation process using native chamomile enzymes to hydrolyze bound forms of apigenin to free aglycone. The contents of apigenin and apigenin-7-O-β-glucoside were determined in both fermented and nonfermented samples by UHPLC-MS–MS analysis to define the efficiency of conversion. After defining their chemical profiles, the extracts of fermented and nonfermented chamomile samples were also compared with respect to their antioxidant, antimicrobial and cytotoxic effects. The antioxidant effects of the obtained extracts were defined by electron spin resonance analysis for hydroxyl and superoxide radicals. The antimicrobial activity was defined for eight microbial strains, whereas cytotoxic activity was evaluated using two human cell lines (human cervix carcinoma and human rhabdomyosarcoma) and murine fibroblasts.

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References

  • Albuquerque ACL, Pereira MSV, Pereira JV, Pereira LF, Silva DF, Macedo CMR, Higino JS (2010) Antiadherent effect of the extract of the Matricaria recutita L. on microorganisms of dental biofilm. Rev Odontol UNESP 39:21–25

    Google Scholar 

  • Aleksic V, Knezevic P (2014) Antimicrobial and antioxidative activity of extracts and essential oils of Myrtus communis L. Microbiol Res 169:240–254

    Article  CAS  PubMed  Google Scholar 

  • Barros L, Carvalho AM, Morais JS, Ferreira ICFR (2010) Strawberry-tree, blackthorn and rose fruits: detailed characterisation in nutrients and phytochemicals with antioxidant properties. Food Chem 120:247–254

    Article  CAS  Google Scholar 

  • Batista ALA, Diógenes Alves Uchôa Lins R, de Souza Coelho R, do Nascimento Barbosa D, Moura Belém N, Alves Celestino FJ (2014) Clinical efficacy analysis of the mouth rinsing with pomegranate and chamomile plant extracts in the gingival bleeding reduction. Complement Ther Clin Pract 20:93–98

    Article  PubMed  Google Scholar 

  • Baviskar BA, Khadabadia SS, Deore SL, Shiradkar MR (2012) Synthesis of clubbed Triazolyl Indeno[1,2-C]Isoquinolines as an Novel Anticancer Agent. Der Pharmacia Sinica 3:24–30

    CAS  Google Scholar 

  • Calliste CA, Trouillas P, Allais DP, Simon A, Duroux JL (2001) Free radical scavenging activities measured by electron spin resonance study and B16 cell antiproliferative behaviors of seven plants. J Agric Food Chem 49:3321–3327

    Article  CAS  PubMed  Google Scholar 

  • Calliste CA, Trouillas P, Allais DP, Duroux JL (2005) Castanea sativa Mill. Leaves as new sources of natural antioxidant: an electron spin resonance study. J Agric Food Chem 53:282–288

    Article  CAS  PubMed  Google Scholar 

  • Čanadanović-Brunet J, Djilas S, Ćetković G, Tumbas V (2005) Free-radical scavenging activity of wormwood (Artemisia absinthium L.) extracts. J Sci Food Argic 85:265–273

    Article  Google Scholar 

  • Čanadanović-Brunet J, Ćetković G, Djilas S, Tumbas V, Savatović S, Mandić A, Markov S, Cvetković D (2009) Radical scavenging and antimicrobial activity of horsetail (Equisetum arvense L.) extracts. Int J Food Sci Technol 44:269–278

    Article  Google Scholar 

  • Cushnie TPT, Lamb AJ (2005) Review: antimicrobial activity of flavonoids. Int J Antimicrob Agents 26:343–356

    Article  CAS  PubMed  Google Scholar 

  • Cuvelier ME, Richard H, Berset C (1992) Comparison of the antioxidative activity of some acid-phenols: structure-activity relationship. Biosci Biotech Biochem 56:324–325

    Article  CAS  Google Scholar 

  • Cvetanović A, Švarc-Gajić J, Mašković P, Savić S, Nikolić Lj (2014) Antioxidant and biological activity of chamomile extracts obtained by different techniques: perspective of using superheated water for isolation of biologically active compounds. Ind Crop Prod. In Press

  • Dai J, Mumper RJ (2010) Plant Phenolics: extraction, analysis and their antioxidant and anticancer properties. Molecules 15:7313–7352

    Article  CAS  PubMed  Google Scholar 

  • Đaković S, Ilić S, Cvejić J, Antanacković M, Antov M, Zeković Z (2008) Camomile autofermentation in polyethylene glycol/dextran two-phase system. Acta periodica technologica 39:133–138

    Google Scholar 

  • Dighe RD, Shiradkara MR, Rohomb SS, Dighe PD (2011) Synthesis and SAR of methyl linked cyclohexyl thiophenyl triazoles for their Anti-Alzheimer activity. Der Chemica Sinica 2:70–87

    CAS  Google Scholar 

  • Dragland S, Senoo H, Wake K, Holte K, Blomhoff R (2003) Several culinary and medicinal herbs are important sources of dietary antioxidants. J Nutr 133:1286–1290

    CAS  PubMed  Google Scholar 

  • Egea I, Sanchez-Bel P, Romajaro F, Pretel MT (2010) Replace synthetic additives in functional foods as a natural antioxidant. Plants Foods Hum Nutr 65:121–129

    Article  CAS  Google Scholar 

  • Fattahi M, Nazeri V, Torras-Claveria L, Sefidkon F, Cusido RM, Zamani Z, Palazon J (2013) Identification and quantification of leaf surface flavonoids in wild-growing populations of Dracocephalum kotschyi by LC–DAD–ESI-MS. Food Chem 141:139–146

    Article  CAS  PubMed  Google Scholar 

  • Fotsis T, Pepper MS, Aktas E, Breit S, Rasku S, Adlercreutz H, Wahala K, Montesano R, Schweigerer L (1997) Flavonoids, dietary-derived inhibitors of cell proliferation and in vitro angiogenesis. Cancer Res 57:2916–2921

    CAS  PubMed  Google Scholar 

  • Franke R, Schilcher H (2005) Chamomile: Industrial Profiles, II Series: Medicinal and Aromatic Plants, vol 42. CRC Press/Taylor & Francis Group, Boca Raton/Broken Sound Parkway

    Google Scholar 

  • Galleano M, Verstraeten SV, Oteiza PI, Fraga CG (2010) Antioxidant actions of flavonoids: thermodynamic and kinetic analysis. Arch Biochem Biophys 501:23–30

    Article  CAS  PubMed  Google Scholar 

  • Guimarães R, Barros L, Dueñas M, Calhelha RC, Carvalho AM, Santos-Buelga C, Queiroz MJRP, Ferreira ICFR (2013) Infusion and decoction of wild German chamomile: bioactivity and characterization of organic acids and phenolic compounds. Food Chem 136:947–954

    Article  PubMed  Google Scholar 

  • Kečkeš S, Gašić U, Ćirković-Veličković T, Milojković-Opsenica D, Natić M, Tešić Ž (2013) The determination of phenolic profiles of Serbian unifloral honeys using ultra-high-performance liquid chromatography/high resolution accurate mass spectrometry. Food Chem 138:32–40

    Article  PubMed  Google Scholar 

  • Kilicgun H, Altiner D (2010) Correlation between antioxidant effect mechanisms and polyphenol content of Rosa canina. Phcog Mag 6:238–241

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kurćubić V, Mašković P, Vujić J, Vranić D, Vesković-Moračanin S, Okanović Đ, Lilić S (2014) Antioxidant and antimicrobial activity of Kitaibelia vitifolia extract as alternative to the added nitrite in fermented dry sausage. Meat Sci 97:459–467

    Article  PubMed  Google Scholar 

  • Lee KG, Shibamoto T (2002) Determination of antioxidant potential of volatile extracts isolated from various herbs and spices. J Agric Food Chem 50:4947–4952

    Article  CAS  PubMed  Google Scholar 

  • Li B, Birt DF (1996) In vivo and in vitro percutaneous absorption of cancer preventive flavonoid apigenin in different vehicles in mouse skin. Pharm Res (NY) 13:1710–1715

    Article  CAS  Google Scholar 

  • Lis-Balchin M, Deans SG, Eaglesham E (1998) Relationship between bioactivity and chemical composition of commercial essential oils. Flavour Frag J 13:98–104

    Article  CAS  Google Scholar 

  • Liu LZ, Fang J, Zhou Q, Hu X, Shi X, Jiang BH (2005) Apigenin inhibits expression of vascular endothelial growth factor and angiogenesis in human lung cancer cells: implication of chemoprevention of lung cancer. Mol Pharmacol 68:635–643

    CAS  PubMed  Google Scholar 

  • Maier R, Kreis W, Carle R, Reinhard E (1991) Partial purification and substrate specificity of a β-glucosidase from Chamomilla recutita. Planta Med 57:A84–A85

    Article  Google Scholar 

  • Mann C, Staba EJ (1986) The chemistry, pharmacology, and commercial formulations of chamomile. In: Craker LE, Simon JE (eds) Herbs, spices, and medicinal plants: recent advances in botany, horticulture, and pharmocology. Oryx, phoenix, pp 235–280

  • Manojlović N, Ranković B, Kosani M, Vasiljević P, Stanojković T (2012) Chemical composition of three Parmelia lichens and antioxidant, antimicrobial and cytotoxic activities of some their major metabolites. Phytomedicine 19:1166–1172

    Article  PubMed  Google Scholar 

  • Mark SB (2004) The role of natural product chemistry in drug discovery. J Nat Prod 67:2141–2153

    Article  Google Scholar 

  • Mckay DL, Blumberg JB (2006) A review of the bioactive and potential health benefits of chamomile tea (Matricaria recutita L.). Phytother Res 20:519–530

    Article  CAS  PubMed  Google Scholar 

  • Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55–63

    Article  CAS  PubMed  Google Scholar 

  • Newman DJ, Gragg GM (2007) Natural products as sources of new drugs over the last 25 years. J Nat Prod 70:461–477

    Article  CAS  PubMed  Google Scholar 

  • Okuno T, Kawai H, Hasegawa T, Ueno H, Nakamuro K (2001) Enhancement of hydroxyl radical formation from superoxide anion radical in the presence of organic selenium compounds. J Health Sci 47:240–247

    Article  CAS  Google Scholar 

  • Oliveira I, Sousa A, Ferreira ICFR, Bento A, Estevinho L, Pereira JA (2008) Total phenols, antioxidant potential and antimicrobial activity of walnut (Juglans regia L.) green husks. Food Chem Toxicol 46:2326–2331

    Article  CAS  PubMed  Google Scholar 

  • Patel D, Shukla S, Gupta S (2007) Apigenin and cancer chemoprevention: progress, potential and promise. Int J Oncol 30:233–245

    CAS  PubMed  Google Scholar 

  • Pekić B, Zeković Z (1994) Investigation of Chamomile fermentation. Biotechnol Lett 16:1323–1328

    Google Scholar 

  • Pekić B, Lepojević Ž, Slavica B (1989) Determination of apigenin and apigenin-7-O-β-glucoside in the Matricaria chamomilla ligulate flowers. Arh Farm 39:169–174

    Google Scholar 

  • Pekić B, Zeković Z, Lepojević Ž (1994) Investigation of apigenin-7-O-β-glucoside hydrolysis by β-glucosidase from almonds. Biotechnol Lett 16:229–234

    Article  Google Scholar 

  • Pereira JA, Pereira APG, Ferreira ICFR, Valentão P, Andrade PB, Seabra R, Estevinho L, Bento A (2006) Table olives from Portugal: phenolic compounds, antioxidant potential and antimicrobial activity. J Agric Food Chem 54:8425–8431

    Article  CAS  PubMed  Google Scholar 

  • Pereira AP, Ferreira ICFR, Marcelino F, Valentão P, Andrade F, Seabra R, Estevinho L, Bento A, Pereira JA (2007a) Phenolic compounds and antimicrobial activity of olive (Olea europaea L. Cv. Cobrancosa) leaves. Molecules 12:1153–1162

    Article  CAS  PubMed  Google Scholar 

  • Pereira JA, Oliveira I, Sousa A, Valentão P, Andrade PB, Ferreira ICFR, Ferreres F, Bento A, Seabra R, Estevinho L (2007b) Walnut (Juglans regia L.) leaves: phenolic compounds, antimicrobial activity and antioxidant potential of different cultivars. Food Chem Toxicol 45:2287–2295

    Article  CAS  PubMed  Google Scholar 

  • Petronilho S, Maraschin M, Coimbra MA, Rochaa SM (2012) In vitro and in vivo studies of natural products: a challenge for their valuation. The case study of chamomile (Matricaria recutita L.). Ind Crop Prod. 40:1–12

    Article  CAS  Google Scholar 

  • Proestos C, Chorianopoulos N, Nychas GJE, Komaitis M (2005) RP-HPLC analysis of the phenolic compounds of plant extracts. Investigation of their antioxidant capacity and antimicrobial activity. J Agric Food Chem 53:1190–1195

    Article  CAS  PubMed  Google Scholar 

  • Rauha JP, Remes S, Heinonen M, Hopia A, Kähkönen M, Kujala T, Pihlaja K, Vuorela H, Vuorela P (2000) Antimicrobial effects of Finnish plant extracts containing flavonoids and other phenolic compounds. Int J Food Microbiol 56:3–12

    Article  CAS  PubMed  Google Scholar 

  • Roby MHH, Sarhan MA, Selim KAH, Khalela KI (2013) Antioxidant and antimicrobial activities of essential oil and extracts of fennel (Foeniculum vulgare L.) and chamomile (Matricaria chamomilla L.). Ind Crop Prod 44:437–445

    Article  CAS  Google Scholar 

  • Satyajit D, Sarker LN, Kumarasamy Y (2007) Microtitre plate based antibacterial assay incorporating resazurin as indicator of cell growth, and its application in the in vitro antibacterial screening of phytochemicals. Methods 42:321–324

    Article  Google Scholar 

  • Shikov AN, Pozharitskaya ON, Makarov VG, Kvetnaya AS (2008) Antibacterial activity of Chamomilla recutita oil extract against Helicobacter pylori. Phytother Res 22:252–253

    Article  PubMed  Google Scholar 

  • Shukla S, Gupta S (2004) Molecular mechanisms for apigenin-induced cell-cycle arrest and apoptosis of hormone refractory human prostate carcinoma DU145 cells. Mol Carcinog 39:114–126

    Article  CAS  PubMed  Google Scholar 

  • Shukla S, Gupta S (2009) Apigenin and cancer chemoprevention. In: Watson RR, Preedy VR (eds) Bioactive foods in promoting health, fruits and vegetables, 1st edn. Elsevier, London, UK, pp 663–689

  • Shukla S, Gupta S (2010) Apigenin: a promising molecule for cancer prevention. Pharm Res 27:962–978

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Soliman KM, Badeaa RI (2002) Effect of oil extracted from some medicinal plants on different mycotoxigenic fungi. Food Chem Toxicol 40:1669–1675

    Article  CAS  PubMed  Google Scholar 

  • Song H, Zhang H, Fu Y, Mo H, Zhang M, Chen J, Li P (2014) Screening for selective inhibitors of xanthine oxidase from Flos Chrysanthemum using ultrafiltration LC–MS combined with enzyme channel blocking. J Chromatogr B 961:56–61

    Article  CAS  Google Scholar 

  • Srivastava JK, Gupta S (2010) Health promoting benefits of chamomile in the elderly population. In: Watson RR (ed) Complementary and alternative therapies and the aging population an evidence-based approach, 1st edn. Elsevier, San Diego, USA, pp 135–157

  • Švarc-Gajić J (2011) Samples and sample preparation in analytical chemistry. Novapublishers, New York

    Google Scholar 

  • Švehlíková V, Bennett RN, Mellon FA, Needs PW, Piacente S, Kroon PA, Bao Y (2004) Isolation, identification and stability of acylated derivatives of apigenin 7-O-glucoside from chamomile (Chamomilla recutita [L.] Rauschert). Phytochemistry 65:2323–2332

    Article  PubMed  Google Scholar 

  • Tekwu EM, Pieme AC, Beng VP (2012) Investigations of antimicrobial activity of some Cameroonian medicinal plant extracts against bacteria and yeast with gastrointestinal relevance. J Ethnopharmacol 142:265–273

    Article  PubMed  Google Scholar 

  • Tumbas V, Čanadanovic-Brunet J, Gille L, Ðilas S, Ćetković G (2010) Superoxide anion radical scavenging activity of bilberry (Vaccinium myrtillus L.). J Berry Res 1:13–23

    Google Scholar 

  • Vieira DRP, Amaral FMM, Maciel MCG, Nascimento FRF, Libério SA, Rodrigues VP (2014) Plant species used in dental diseases: ethnopharmacology aspects and antimicrobial activity evaluation. J Ethnopharmacol 155:1441–1449

    Article  PubMed  Google Scholar 

  • Wang IK, Lin-Shiau SY, Lin JK (1999) Induction of apoptosis by apigenin and related flavonoids through cytochrome c release and activation of caspase-9 and caspase-3 in leukaemia HL-60 cells. Eur J Cancer 35:1517–1525

    Article  CAS  PubMed  Google Scholar 

  • Wang W, VanAlstyne PC, Irons KA, Chen S, Stewart JW, Birt DF (2004) Individual and interactive effects of apigenin analogs on G2/M cell-cycle arrest in human colon carcinoma cell lines. Nutr Cancer 48:106–114

    Article  CAS  PubMed  Google Scholar 

  • Ye JX, Wei W, Quan LH, Liu CY, Chang Q, Liao YH (2010) An LC–MS/MS method for the simultaneous determination of chlorogenic acid, forsythiaside A and baicalin in rat plasma and its application to pharmacokinetic study of Shuang-huang-lian in rats. J Pharm Biomed Anal 52:625–630

    Article  CAS  PubMed  Google Scholar 

  • Yin F, Giuliano AE, Van Herle AJ (1999) Growth inhibitory effects of flavonoids in human thyroid cancer cell lines. Thyroid 9:369–376

    Article  CAS  PubMed  Google Scholar 

  • Yin F, Giuliano AE, Law RE, Van Herle AJ (2001) Apigenin inhibits growth and induces G2/M arrest by modulating cyclin-CDK regulators and ERK MAP kinase activation in breast carcinoma cells. Anticancer Res 21:413–420

    CAS  PubMed  Google Scholar 

  • Zekovic Z (1993) Determination of extraction and chemical transformations of flavonoids of chamomile (Matricaria chamomilla L.), Master thesis, Novi Sad

  • Zhang J, Chen M, Ju W, Liu S, Xu M, Chu J, Wu T (2010) Liquid chromatograph/tandem mass spectrometry assay for the simultaneous determination of chlorogenic acid and cinnamic acid in plasma and its application to a pharmacokinetic study. J Pharm Biomed Anal 51:685–690

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The present work was carried out within the project of the Serbian Ministry of Education, Science and Technological Development (Project No. TR 31013). The authors are grateful to dr Dušan Adamović, Institute of Field and Vegetable Crops, Bački Petrovac, Serbia, for his support in supplying plant material.

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Cvetanović, A., Švarc-Gajić, J., Zeković, Z. et al. Comparative analysis of antioxidant, antimicrobiological and cytotoxic activities of native and fermented chamomile ligulate flower extracts. Planta 242, 721–732 (2015). https://doi.org/10.1007/s00425-015-2308-2

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