Composition and Antimicrobial Activity of Celery (Apium graveolens) Leaf and Root Extracts Obtained with Liquid Carbon Dioxide
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1 Composition and Antimicrobial Activity of Celery (Apium graveolens) Leaf and Root Extracts Obtained with Liquid Carbon Dioxide A. Sipailiene and P.R. Venskutonis Department of Food Technology Kaunas University of Technology Lithuania A. Sarkinas and V. Cypiene Lithuanian Food Institute Kaunas Lithuania Keywords: essential oil, extract yield, carvone, limonene, phthalides Abstract Dried roots and leaves of celery were extracted with liquid carbon dioxide in the pilot plant scale equipment. In total, 9 extractions of roots and 4 extractions of leaves were performed at ambient temperature and 60 bar pressure by using different operation cycle programs. Extract yields were up to 1.6% both from roots and leaves. Volatile compounds were hydrodistilled from the extracts in a Clevenger type apparatus and their composition was analysed by capillary gas chromatography and mass spectrometry (GC/MS). The main constituents in the oil of roots were limonene, carvone and 3n-butylphthalide. The essential oil of leaves contained higher amount of limonene comparing to the roots, and very small amount of carvone. Other differences in the volatile oil composition between roots and leaves also were observed. The extracts were tested on the following microorganisms: Escherichia coli, Listeria monocytogenes, Citrobacter freundii, Hafnia alvei, Salmonella typhimurium, Bacillus cereus, Enterococcus faecalis, Enterobacter aerogenes, Staphylococcus aureus and Proteus vulgaris. The antimicrobial effect was assessed using agar diffusion method by applying ethanolic solutions of extracts. It was found that all the investigated leaf extracts were effective inhibitors of H. alvei, S. aureus, E. coli, Bac. cereus, E. faecalis and E. aerogenes, however the extracts isolated from the roots were less effective; all of them possessed high activity only against B. cereus and E. faecalis. C. freundii and P. vulgaris were resistant against celery extracts isolated both from roots and leaves. INTRODUCTION The antimicrobial properties of spices and aromatic herbs have been tested in numerous studies, including their role as a natural method of food preservation. Biological properties of different anatomical parts of celery and its extracts were reported in various literature sources (Bedin et al., 1999). Celery had potent antimicrobial activity against Bacillus subtilis, Escherichia coli and Saccharomyces cerevisiae (Krishna and Banerjee, 1999); celery seed oil was active against Campylobacter jejuni (Friedman et al., 2002), celery essential oil inhibited various pathogenic and saprophytic microorganisms (Elgayyar et al., 2001). However, in some cases it was reported that essential oil of celery was inactive or had little activity (Kivanc and Akgul, 1986). Various biologically active compounds were identified in celery essential oils and extracts. For instance, sedanolide and two senkyunolides were active against nematode, mosquito larvae and fungi (Momin and Nair, 2001), furanocoumarins inhibited Listeria monocytogenes, Escherichia coli O157:H7, and Micrococcus luteus (Ulate-Rodrigues et al., 1997). Plant extracts can be obtained by different extraction methods with various solvents. Extraction with liquid and supercrititical gases provides several important advantages, which were thoroughly discussed in numerous literature sources (Moyler, 1993). This method has also been used with Umbelliferae family plants, including celery (Catchpole et al., 1996; Dauksas et al., 2002). It is interesting to note that the yields of steam distilled oil and isolated by liquid CO 2 extracts from celery seeds were almost equal and constituted % and 3% respectively, whereas in case of parsley seeds % of oil were distilled by steam during 5 h, and 9.8% of the extract were obtained by Proc. WOCMAP III, Vol. 3: Perspectives in Natural Product Chemistry Eds. K.H.C. Başer, G. Franz, S. Cañigueral, F. Demirci, L.E. Craker and Z.E. Gardner Acta Hort. 677, ISHS
2 CO 2 during 2 hours of extraction at 58 bar and 20 C (Moyler, 1994). The goal of this study was to prepare celery leaf and root extracts with liquid carbon dioxide and to determine extract yields, composition and antimicrobial activity. MATERIALS AND METHODS The company Meta provided dried celery (Apium graveolens L.) leaves and roots. They were comminuted in a hammer mill and extracted in a pilot plant at company Stumbras, Lithuania. Carbon dioxide extraction unit (Fig. 1) operated at ambient temperature and a pressure of 60 bar. The main extraction cycle consisted of the three steps: (i) filling of the extractor containing ground raw material with liquid CO 2 ; (ii) maceration of raw material with solvent; (iii) solvent removal and extract collection at 40 C. The antimicrobial properties were evaluated by diffusion method into the agar. Ten undesirable in food products species, namely Escherichia coli, Listeria monocytogenes, Citrobacter freundii, Hafnia alvei, Salmonella typhimurium, Bacillus cereus, Enterococcus faecalis, Enterobacter aerogenes, Staphylococcus aureus and Proteus vulgaris, were used as test cultures. Bacteria were grown on the plate count agar (LAB 98, LAB M) 24 hours at 37 C. After cultivation test culture cells were washed with saline and cell suspensions were prepared according to McFarland standard. The suspension of bacteria cells was introduced into the dissolved and cooled to 47 C media, 10 ml of which were pipetted into a 90 mm diameter Petri plate. Nine-millimetre diameter wells were pushed in the agar and filled with 1, 5 or 10% solutions of extracts. The plates were incubated overnight at 37 C temperature, and the clear zone of inhibition (mm) was measured. The content of the essential oil in ground roots, leaves and CO 2 -extracts was determined in European Pharmacopoeia apparatus. Composition of essential oils was analysed by capillary gas chromatography (GC) and coupled gas chromatography-mass spectrometry (GC/MS). Essential oils were diluted in diethyl ether (20 µl in 1 ml) and analysed with Fisons 8261 gas chromatograph equipped with flame ionisation detector (FID) on a fused silica capillary column DB-5, 25 m length, 0.32 mm i.d., and 0.5 µm film thickness. Helium was used as a carrier gas with a flow rate of 1.6 ml/min; detector temperature was 260 C, oven temperature was programmed from 40 C to 250 C at the rate of 4 C min -1. Split injector was heated at 250 C, split ratio was 15:1. Data was processed on a DP 800 integrator. For the identification essential oils were analysed on a HP 5890 (II) instrument equipped with a 5971 series mass selective detector in the electron impact ionisation mode at 70eV, and the following GC parameters: split inlet 1:10; helium as a carrier gas at a flow rate of 2 ml min -1 ; fused silica HP5 MS column (Hewlett Packard, crosslinked 5% phenyl methyl silicone) 30 m length, 0.25 mm id, 0.25 µm film thickness, temperature program from 40 to 250 C increasing at 4 C min -1. Identification was based mainly on the comparison of retention indices (Adams, 2001) and mass spectra (NIST/EPA/NIH Mass Spectral Database NBS75K). RESULTS AND DISCUSSION Extraction results are summarised in Table 1. Extract yields varied from 0.52 to 1.59% from the roots and from 0.56 to 1.26% from the leaves. So far as it was not possible to change the pressure and the temperature in the pilot extractor, three main factors could have an influence on the extraction yield: quality of raw material, fineness of particles and extraction procedure. It was observed that additional grinding of raw material in the hammer mill increased the yield. It is known that hydrophobic essential oil substances are soluble in liquid carbon dioxide, therefore it can be expected that major part of the oil will be isolated from the plant material. The content of the essential oil in celery roots was very low, actually it was difficult to distil measurable amount of oil from 100 g of ground roots by the standard method. Celery root and leaf extracts contained higher amounts of oil and it confirms that extraction with liquid carbon dioxide is suitable 72
3 method to concentrate essential oil components. Composition of Volatile Compounds in the Extracts The composition of volatile constituents in root and leaf extracts is provided in Table 2. The main constituents in celery essential oils were terpenes, sesquiterpenes and phthalides. Limonene was the major constituent both in root and leaf volatile oil, however it was more abundant in the leaves (>30%). Very high amount of other aliphatic terpene, myrcene was characteristic to leaf oils, while in the root oil it constituted less than 0.2%. The content of 3n-butylphthalide, which was the major phthalide group component was almost equal in root and leaf extracts. Considerable amounts of other phthalides, mainly sedanenolide and sedanolide were determined in the roots. These two phthalides were not detected in the leaf extract. The content of carvone was the main quantitatively differentiating factor in the composition of two oils. This compound was abundant in the root extracts (>17%), while in the leaves it was a trace constituent (<0.2%). Higher content of sesquiterpenes in the leaf essential oil has to be mentioned; for instance, the content of three identified selinenes exceeded 9% in the leaf oil. In the root oil, β- selinene, which was a single selinene isomer constituted up to 1.5%. Also, the contents of α-humulene and β-caryophyllene were considerably higher in the leaf oil. Antibacterial Effect of Celery Extracts Results presented in Table 3 show that celery leaf and root extracts in most cases inhibited bacterial growth in the test cultures. However, P. vulgaris and C. freundii were resistant to all celery extracts at the applied concentrations. B. cereus was the most sensitive bacteria to celery extracts; inhibition was observed at the all applied concentrations of the all extracts used in the study. In general, higher concentrations of the extracts had bigger effect on bacteria. In some cases concentration was not an important factor, even comparing 1 and 10% concentrations (e.g., B. cereus, leaf extract, batch no. 3; S. aureus, leaf extract, batch no. 1). The differences between extraction batches have also been observed. For instance, leaf extracts from batches no. 1 and no. 2 did not have any effect on L. monocytogenes, whereas, batch no. 3 inhibited the growth of these pathogens at the all concentrations applied. Root extract from the batch no. 1 had the effect only on L. monocytogenes and E. faecalis (10%), while root extract from the batch no. 3 inhibited all tested bacteria except for C. freundii and P. vulgaris. Crude extracts are complex mixtures containing various compounds, both active and having no effect on microorganisms. CONCLUSIONS Liquid carbon dioxide is suitable solvent for the extraction of celery volatile constituents, however, the yields of the extracts were not high, most likely due to a low amount of essential oil and other soluble constituents at the CO 2 parameters applied. Limonene and 3n-butylphthalide were important components of volatile fractions distilled from celery roots and leaves. High amounts of myrcene and some sesquiterpenes were characteristic to leaf extracts, root extracts contained high percentage of carvone. Leaf extracts were more active antimicrobial agents compared to root extracts. P. vulgaris and C. freundii were most resistant to celery extracts, while the growth of B. cereus was inhibited by all extracts at the all applied concentrations. Literature Cited Adams, R.P Identification of Essential Oil Components by Gas Chromatography/ Quadrupole Mass Spectroscopy. Allured Publishing, USA. Bauermann, U., Ehrich, J. and Thomann, R. [Herb essential oils.] Aetherische Krautoele. Lebensmitteltechnik 26: Bedin, C., Gutkoski, S.B. and Wiest, J.M Antimicrobial activity of spices. Higiene Alimentar. 13:26-29 (Portuguese). Catchpole, O.J., Grey, J.B. and Smallfield, B.M Near-critical extraction of sage, 73
4 celery, and coriander seed. J. Supercrit. Fluids 9: Dauksas, E., Venskutonis, P.R., Sivik, B. and Nillson, T Effect of fast CO 2 pressure changes on the yield of lovage (Levisticum officinale Koch.) and celery (Apium graveolens L.) extracts. J. Supercrit. Fluids 22: Elgayyar, M., Draughon, F.A., Golden, D.A. and Mount, J.R Antimicrobial activity of essential oils from plants against selected pathogenic and saprophytic microorganisms. J. Food Protect. 64: Friedman, M., Henika, P.R. and Mandrell, R.E Bactericidal activities of plant essential oils and some of their isolated constituents against Campylobacter jejuni, Escherichia coli, Listeria monocytogenes, and Salmonella enterica. J. Food Protect. 65: Momin, R.A. and Nair, M.G Mosquitocidal, nematicidal, and antifungal compounds from Apium graveolens L. seeds. J. Agric. Food Chem. 49: Moyler, D Extraction of flavours and fragrances with compressed CO 2. p In: M.B. King and T.R. Bott (eds.), Extraction of Natural Products Using Near- Critical Solvents. Blackie A&P, London. Moyler, D Spices - recent advances. p In: G. Charalambous (ed.), Developments in Food Science 34, Spices, Herbs and Edible Fungi, Elsevier Science Publishers, Amsterdam. Kivanc, M. and Akgul, A Antibacterial activities of essential oils from Turkish spices and citrus. Flav. Fragr. J. 1: Krishna, de A.M. and Banerjee, A.-B Antimicrobial screening of some Indian spices. Phytother. Res. 13: Ulate-Rodrigues, J., Schafer, H.W., Zottola, E.A. and Davidson, P.M Inhibition of Listeria monocytogenes, Escherichia coli O157:H7, and Micrococcus luteus by linear furanocoumarins in culture media. J. Food Protect. 60: Tables Table 1. Celery extraction parameters and extract yields. Extraction Number of extraction cycles Extraction cycle* time, min Extract yield, % Essential oil content in the extract, % Roots 1 batch Roots 2 batch Roots 3 batch Roots 4 batch Roots 5 batch Roots 6 batch Roots 7 batch Roots 8 batch Roots 9 batch Leaves 1 batch Leaves 2 batch Leaves 3 batch Leaves 4 batch * Extraction cycle = extractor filling with carbon dioxide + raw material maceration 74
5 Table 2. Composition (%) of volatile fraction of celery root and leaf extracts. Constituent Root Leaf Constituent Root Leaf α-pinene Myrtenyl acetate (t) 0.14 nd Camphene 0.16 nd E-Carvyl acetate nd 0.15 β-pinene γ-nonalactone (t) 0.17 nd Myrcene α-cubebene nd 0.11 Ethyl hexanoate 0.10 nd α-copaene nd 0.24 Octanal 0.25 nd 1-Tetradecene 0.39 nd Methyl heptanoate nd 0.63 Methyl undecanoate nd nd Limonene Tetradecane 0.35 nd cis-β-ocimene 0.46 nd β-caryophyllene trans-β-ocimene nd 0.28 α-humulene γ-terpinene allo-aromadendrene 0.24 nd Methyl octanoate nd epi-trans nd Caryophyllene (t) Fenchone 0.17 nd Germacrene D nd 0.68 Linalool 1.63 nd β-selinene neo-allo-ocimene nd 0.15 δ-selinene nd 5.98 Limonene oxide nd 0.13 α-selinene nd 1.34 Camphor 0.13 nd Neryl propanoate (t) nd 0.42 Pentyl benzene γ-cadinene nd 0.48 Menthol 0.47 nd δ-cadinene nd 0.62 Ethyl octanoate 0.25 nd Caryophyllene oxide trans-carveol nd n-Butylphthalide Carvone cis-3n Butylidenephthalide 2-trans-Decenal 0.23 nd Unknown 3.39 nd Methyl nonanoate nd 0.08 Sedanenolide 4.77 nd Isobornyl acetate 1.31 nd Sedanolide 7.01 nd 2-trans,4-cis-Decadienal 0.30 nd Octadecane 0.31 nd 2-Undecanone nd 0.13 Ethyl hexadecanoate 2.38 nd 2-trans,4-trans nd cis-falcarinol (t) 1.69 nd Decadienal Methyl decanoate nd 0.21 Methyl linoleate 1.61 nd nd = not detected; t = tentatively identified (based on a good match of mas spectrum) 75
6 Table 3. Inhibition of various microorganisms by celery leaf and root extracts, mm inhibition zone. Extract Concentraction Hafnia alvei Salmonella typhimurium Staphylococcus aureus Escherichia coli Listeria monocytogenes Bacilus cereus Enterococcus faecalis Citrobacter freundii Enterobacter aerogenes Proteus vulgaris Leaves 10% 17.5± ± ± ± ± ± ± ±0.7 - batch 5% ± ± ± ± ± ±1.4 - no. 1 1% ± ± ± ± ± ±0.7 - Leaves 10% 17.5± ± ± ± ± ± ±0.0 - batch 5% 13.0± ± ± ± ± ± ±0.7 - no. 2 1% 9.0± ± ± ± ± Leaves 10% 25.5± ± ± ± ± ± ±2.1 - batch 5% 16.5± ± ± ± ± ± ±0.7 - no. 3 1% ± ± ± ± ± Roots 10% ± ± batch 5% ± no. 1 1% ± Roots 10% 11.0± ± ± ± ± ±0.0 - batch 5% ± ± ± no. 2 1% ± ± ± Roots 10% 12.0± ± ± ± ± ± ± ±0.0 - batch 5% 11.0± ± ± ± ± ± ± no. 3 1% ± ± ± ± ±
7 Figures Condenser CO 2 tank Extractor Extract separator Fig. 1. Carbon dioxide extraction equipment. 77
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