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Annulatum MORIS and Hypericum Elegans JELENA S

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Annulatum MORIS and Hypericum Elegans JELENA S Available on line at Association of the Chemical Engineers of Serbia AChE www.ache.org.rs/CICEQ Chemical Industry & Chemical Engineering Quarterly 19 (1) 7−11 (2013) CI&CEQ ALEKSANDRA S. ANTIMICROBIAL ACTIVITY OF Hypericum ĐORĐEVIĆ1 2 annulatum MORIS AND Hypericum elegans JELENA S. LAZAREVIĆ STEPHAN EX WILLD. ESSENTIAL OILS VIOLETA D. MITIĆ1 RADOSAV M. PALIĆ1 FROM SERBIA GORDANA S. The in vitro antimicrobial activity of Hypericum annulatum and Hypericum ele- STOJANOVIĆ1 gans essential oils was evaluated against a panel of standardized bacteria and 1Department of Chemistry, Faculty fungi using broth microdilution assay. Both essential oils showed antimicrobial of Science and Mathematics, activity against all the tested microorganisms. Hypericum annulatum essential University of Niš, Niš, Serbia oil showed better antibacterial than antifungal activity, being more effective 2 Department of Pharmacy, Faculty against Pseudomonas aeruginosa and Escherichia coli while H. elegans es- of Medical Sciences, University of sential oil showed no significant difference between antibacterial and anti- Niš, Niš, Serbia fungal activity. Antimicrobial testing of α-pinene, β-pinene and β-myrcene com- SCIENTIFIC PAPER pounds was also performed. All the compounds were active against all the tested microorganisms, however, based on the MIC, MBC and MFC values, UDC 615.322/.33:633.8(497.11) none of these compounds could be thought of as the main bearer of the oils’ antimicrobial activity. This is the first report regarding the antimicrobial activity DOI 10.2298/CICEQ120111036D of the essential oils of the two Hypericum species. Keywords: Hypericum annulatum, Hypericum elegans, essential oil, antimicrobial activity. Hypericum L. (Hypericaceae) is a genus repre- antiviral and antidepressant activity), tannins (anti- sented by more than 400 species, widespread in viral, antimicrobial and antioxidant activity), flavonoids warm-temperate areas throughout the world, as well (antifungal, antioxidant and antidepressant activity) as on the Balkan Peninsula [1]. Plants of the genus and volatile oils (antimicrobial activity) [16-19]. Hype- Hypericum have traditionally been used as highly ricum annulatum Moris (syn.: Hypericum atomarium esteemed medicinal plants [2]. Among these, H. per- Boiss. subsp. degenii (Bornm.) Hayek and Hypericum foratum is one of the best chemically investigated degenii Bornm.) is no exception in this respect. This plant species. The volatile profiles of the other related species’ natural habitats are slightly inclined, shady Hypericum species, including those originating from and hilly slopes shielded from strong wind. In Serbia southeastern Serbia, have been investigated [3-9]. this plant grows mostly on siliceous geological sub- The extracts, as well as the essential oil of Hy- stratum, but it also inhabits limestone habitats. pericum species have been shown to possess signi- Hypericum annulatum subsp. annulatum is used in ficant antiviral, wound healing, antioxidant and anti- folk medicine for the treatment of gastric and liver microbial activities [4,7,10-15]. Some of these actions disorders [20]. Recent investigations on several ben- were attributed to the presence of phloroglucinols zophenone glycosides and xanthones isolated from (antibacterial, wound healing, antimalarial and antide- aerial parts of H. annulatum indicate their potential pressant activity), naphthodianthrones (antiviral and chemoprotective/radioprotective properties as well as antidepressant activity), xanthones (antimicrobial, their protective effect against some toxic agents [21,22]. A new isocoumarin from H. annulatum, annu- latomarin, exhibited a modest growth-inhibitory acti- Correspondence: A.S. Đorđević, Department of Chemistry, vity in vitro against human chronic myeloid leukemia Faculty of Science and Mathematics, University of Niš, Više- [23]. A prenylated phloroglucinol, hyperatomarin, also gradska 33, 18000 Niš, Serbia. E-mail: [email protected] a secondary metabolite of H. annulatum, has been Paper received: 11 January, 2012 shown to possess significant antibiotic activity against Paper revised: 21 April, 2012 Gram-positive bacteria [24]. The very scarce literature Paper accepted: 22 April, 2012 7 A.S. ĐORĐEVIĆ et al.: ANTIMICROBIAL ACTIVITY OF Hypericum… CI&CEQ 19 (1) 7−11 (2013) data on H. elegans includes mostly its non-volatile two Gram-positive (Bacillus subtilis ATCC 6633 and chemistry [17,25,26], with no reports on its biological Staphylococcus aureus ATCC 6538) and three Gram- activities. This rare species, in Serbia inhabits xero- negative bacteria (Escherichia coli ATCC 8739, Pseu- thermic habitats, dry meadows, pastures, rocky ter- domonas aeruginosa ATCC 9027 and Salmonella rains, sandy soils and rocks [27]. abony NCTC 6017). The antifungal activity was tested Therefore, the aim of this study was to inves- against two organisms Aspergillus niger ATCC 16404 tigate the antimicrobial potential of H. annulatum and and Candida albicans ATCC 10231. H. elegans essential oils, as well as some of their The minimal inhibitory concentration (MIC) of main constituents. the samples against tested bacteria and fungus/yeast was determined by using a broth microdilution me- EXPERIMENTAL thod according to the recommendations of the Natio- nal Committee for Clinical Laboratory Standards Plant material (NCCLS) [28]. The inocula of the tested strains were Aerial parts of H. annulatum in the flowering and prepared from overnight broth cultures and suspen- beginning of fructiferous phase were collected in the sions were adjusted to 0.5 McFarland standard tur- valley of the river Pčinja (near Trgovište, southeastern bidity. Dimethyl sulphoxide (10%, v/v aqueous solu- Serbia) in July 2008. Voucher specimens were depo- tion) was used to dissolve and to dilute samples. A sited in the Herbarium of Institute of Botany and Bo- stock concentration of all tested samples was pre- tanical Garden “Jevremovac”, University of Belgrade pared at 100 mg/ml. A serial double dilution of the (BEOU), under the acquisition number 16269. Aerial samples was prepared in 96 multi-well microtitre parts of H. elegans in the flowering phase were col- plates, using the method of Sarker et al. [29]. Two lected in the region of the Lalinačka Slatina Salt rows in each plate were used as controls. One row Marsh (Svrljig, near Niš, southeastern Serbia) in July was used as a positive control and contained a broad- 2008. Voucher specimens were deposited in the Her- spectrum antibiotic (doxycycline in a serial dilution of barium of the Faculty of Science and Mathematics, 200–0.05 μg/ml) to determine the sensitivity of Gram- University of Niš, under the acquisition number negative and Gram-positive bacteria and an antimy- 200812. cotic (nystatin in a serial dilution of 50–0.02 μg/ml) to determine the sensitivity of fungi. The other row con- Essential oil isolation tained the solvent as negative control. The minimal Fresh aerial parts, of H. annulatum (400 g) and bactericidal/fungicidal concentration (MBC/MFC) was H. elegans (300 g), were subjected to hydrodistillation determined by spreading the content of each well of for 2.5 h using an original Clevenger-type apparatus the microtitre plate in which colour change occurred and yielded 0.05 and 0.08% (w/w) of pale yellow es- on sterile nutrient agar plates (prepared according to sential oils, respectively. The obtained oils were sepa- the manufacturer’s instructions) set in Petri dishes. rated, dried over anhydrous magnesium sulfate and These plates were incubated at 37 °C for 24 h for stored under appropriate conditions before they were bacteria or at 28 °C for 48 h for fungi. The MBC/MFC tested. was evaluated as the lowest concentration of essen- tial oil at which 99.9% of inoculated microorganisms Chemicals and reagents were killed. Tests were carried out in triplicate. α-Pinene, β-pinene and β-myrcene standards were obtained from Sigma Aldrich (St. Louis, USA). RESULTS AND DISCUSSION Diethyl ether was purchased from Carlo Erba (Italy) while anhydrous magnesium sulfate was purchased The results obtained in the broth microdilution from Merck (Darmstadt, Germany). All chemicals and assay are presented in Tables 1 and 2. The anti- reagents were of analytical grade purity. microbial activities of H. annulatum and H. elegans essential oils were evaluated against five bacterial Broth microdilution assay strains, one mold and one yeast species. The results The in vitro antimicrobial activity of essential oils indicated that the MIC values against tested orga- α β and commercial standards - -pinene, -pinene and nisms ranged between 3.13 and 12.50 mg/ml, while β -myrcene was tested against a panel of laboratory the MBC and MFC values were 50.00 mg/ml and control strains belonging to the American Type Cul- higher, for both of tested oils. The assayed samples ture Collection Maryland, USA (except one, belonging were less effective than the antibiotic/antimycotic to National Collection of Type Cultures, UK, see used as reference standard (Table 1). below). Antibacterial activity was evaluated against 8 A.S. ĐORĐEVIĆ et al.: ANTIMICROBIAL ACTIVITY OF Hypericum… CI&CEQ 19 (1) 7−11 (2013) Table 1. Minimal inhibitory (MIC) and minimal bactericidal/fungicidal concentrations (MBC/MFC) of H. annulatum and H. elegans essen- tial oils; n.t. – not tested H. elegans (mg/ml) H. annulatum (mg/ml) Doxycycline (µg/ml) Nystatin (µg/ml) Microorganism MIC MBC/MFC MIC MBC/MFC MIC MBC MIC MFC B. subtilis 12.50 >50.00 6.25 50.00 1.56 1.56 n.t. n.t. S. aureus 3.13 50.00 3.13 >50.00 0.78 6.25 n.t. n.t. E. coli 3.13 50.00 3.13 50.00 0.78 0.78 n.t. n.t. S. abony 12.50 50.00 12.50 >50.00 6.25 6.25 n.t. n.t. P. aeruginosa 6.25 25.00 3.13 50.00 12.50 12.50 n.t. n.t. C. albicans 3.13 50.00 25.00 >50.00 n.t. n.t. 6.25 6.25 A. niger 6.25 50.00 25.00 >50.00 n.t. n.t. 0.78 0.78 Table 2. Minimal inhibitory (MIC) and minimal bactericidal/fungicidal concentrations (MBC/MFC) of selected constituents of H.
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