Int.J.Curr.Microbiol.App.Sci (2016) 5(1): 306-317
ISSN: 2319-7706 Volume 5 Number 1(2016) pp. 306-317 Journal homepage: http://www.ijcmas.com
Original Research Article http://dx.doi.org/10.20546/ijcmas.2016.501.029 Antimicrobial and Antioxidant Activity of the Leaves, Bark and Stems of Liquidambar styraciflua L. (Altingiaceae)
Graziele Francine Franco Mancarz1*, Ana Carolina Pareja Lobo1, Mariah Brandalise Baril1, Francisco de Assis Franco2 and Tomoe Nakashima1
1Pharmaceutical ScienceDepartment, Universidade Federal do Paraná, Curitiba, PR, Brazil 2Coodetec Desenvolvimento, Produção e Comercialização Agrícola Ltda, Cascavel, PR, Brazil
*Corresponding author
A B S T R A C T
K e y w o r d s The genus Liquidambar L. is the best-known genus of the Altingiaceae Horan family, and species of this genus have long been used for the Liquidambar treatment of various diseases. Liquidambar styraciflua L., which is styraciflua, popularly known as sweet gum or alligator tree, is an aromatic deciduous antioxidant tree with leaves with 5-7 acute lobes and branched stems. In the present activity, study, we investigated the antimicrobial and antioxidant activity of aerial antimicrobial parts of L.styraciflua. Antimicrobial activity was evaluated using the activity, microdilution methodology. The DPPH and phosphomolybdenum methods microdilution method, were used to assess the antioxidant capacity of the samples. The extracts DPPH assay showed moderate or weak antimicrobial activity. The essential oil had the lowest MIC values and exhibited bactericidal action against Escherichia Article Info coli, Enterobacter aerogenes and Staphylococcus aureus. The ethyl acetate fraction and the butanol fraction from the bark and stem showed the best Accepted: antioxidant activity. This study revealed that the essential oil of L. 16 December 2015 styraciflua leaves displays antimicrobial activity and can be used as an Available Online: alternative against pathogenic microorganisms. The extracts and fractions of 10 January 2016 this species have a high antioxidant capacity, revealing new sources of antioxidants for the food and pharmaceutical industries.
Introduction
Infectious diseases are a prominent cause of agents (Silver and Bostian, 1993).Thisability morbidity and mortality worldwide, despite has driven the search for substances with technical and scientific advances. One of the antimicrobial activity in natural products, as main factors responsible for this status is the many secondary metabolites of plants have ability of microorganisms to acquire been proven to have antimicrobial properties mechanisms of resistance to antimicrobial in vitro (Chauhan et al., 2015).
306 Int.J.Curr.Microbiol.App.Sci (2016) 5(1): 306-317
Various degenerative diseases, such as diseases, such as stomach disorders, wounds cancer and Parkinson's disease, can be and cough; however, the essential oil caused by the uncontrolled production of extracted from the leaves is also known to reactive oxygen species. The use of exhibit medicinal properties (Lingbeck et antioxidants to aid in the prevention and al., 2015). treatment of these diseases has been studied due to their potential to reduce oxidative Some studies of species of the genus stress (Sadi et al., 2015). Many medicinal Liquidambar demonstrated antimicrobial plants contain a large number of phenolic potential (Sa diç et al., 2005; Kim et al., compounds, such as flavonoids and tannins, 2008; Lee Y-S et al., 2009); however, no which exhibit antioxidant activity (Araujo et studies have been conducted with the al., 2008), encouraging research in this area. essential oil and extracts of the species L. styraciflua. Some studies demonstrated A little explored family is Altingiaceae antioxidant, antitumor, anticoagulant and Horan, which consists of approximately hepatoprotective activity for the species fifteen species that are divided into three L.orientalis and L.formosona (Wang et al., genera: Liquidambar L., Altingia Noronha 2010; Konno C et al., 1988; Yang et al., and Semiliquidambar HT. Chang (Ickert- 2011). The essential oil of the leaves and Bond and Wen, 2006).The extracts and stem of L. styraciflua has anti-inflammatory resins of plants from this family are used in activity and antioxidant activity with low traditional Chinese and Ayurvedic medicine cytotoxicity (El-Readi et al., 2013), but for the treatment of stomach pain, there are no reports in the literature bronchitis, inflammation, amenorrhea and concerning the antioxidant capacity of skin diseases, such as eczema and scabies extracts and fractions of the aerial parts of (El-Readi et al., 2013). this species.
The genus Liquidambar is the best-known The lack of studies related to this species genus of the family and consists of four encourages this work, which aims to intercontinental species in the temperate evaluate the antimicrobial and antioxidant zone of the northern hemisphere: activity of the extracts, fractions and Liquidambar formosana, Liquidambar essential oil of L.styraciflua. acalycina, Liquidambar orientalis and Liquidambar styraciflua (Ickert-Bond et al., Materials and Methods 2005). One of the species of this genus, L.styraciflua L., which is commonly known Plant Material as sweet gum, red gum, alligator tree and Liquidambar, has a wide natural distribution The botanical material was collected from in the southern and southeastern United specimens of L.styraciflua L., States, extending to Mexico and Central ALTINGIACEAE, which were grown in the America. This organism is a deciduous tree experimental field of the Brazilian that is 20-25m high and has leaves with 5-7 Agricultural Research Corporation, acute lobes that are green in the spring and EMBRAPA Forests (Colombo - PR). The summer but turn purple, red, or yellow in the leaves, bark and stems of L. styraciflua were fall (Lorenzi et al., 2003). More than 10,000 collected during the fall and spring of years ago, Native Americans used the storax 2011/2012. of this species for the treatment of various
307
Int.J.Curr.Microbiol.App.Sci (2016) 5(1): 306-317
The hydroalcoholic extract of the leaves and against the selected microorganisms were the hydroalcoholic extract of the bark and determined in sterile 96-wells or holes (TPP) stems of L. styraciflua were prepared using a according to previously described maceration technique at a moderate methodologies (Ayres et al., 2008; temperature. From these extracts, we Hanamanthagouda et al., 2010; Silva et al., prepared fractions into a separatory funnel 2011), with some modifications. The using the liquid-liquid partition method and recommendations ofClinical and Laboratory solvents with increasing polarity (n-hexane, Standards Institute (2005) were applied. chloroform, ethyl acetate, butanol and ethanol 70%). The hydroalcoholic extracts were added to an initial concentration of 2,000 µg/mL, and The essential oil was extracted from dried the serial dilution procedure was then leaves of L. styraciflua via the performed with the first culture medium to hydrodistillation method, using the obtain decreasing concentrations (2,000 Clevenger apparatus. µg/mL to 15.625 µg/mL). For the essential oil, an initial concentration of 1,000 µg/mL Reagents and Chemicals with the solvent 10%Tween 80 was used, and concentrations of 1,000 µg/mL to 3.9 All chemicals and solvents were purchased µg/mL were obtained by serial dilution with from Sigma Aldrich Co. (St. Louis, MO, medium. USA) and Merck Millipore (Darmstadt, Germany). In the last columns of the plate,we added the positive controls (30 µg/mL of erythromycin Antimicrobial Activity for bacteria; 50 µg/mL of ketoconazole and 50 µg/mL of terbinafine for yeast), the For the antibacterial tests, we selected eight negative controls (solvent) and the sterility standard strains of bacteria from the control for the culture medium. company NEWPROV, including four Gram- positive bacteria and four Gram-negative To verify the ability of the sample to inhibit bacteria. In the antifungal tests, we used five the growth of microorganisms or cause the standard yeast strains from the Mycology death of microorganisms, a methodology Laboratory of Clinical Hospital (Curitiba- described by Veljic et al. (2010) was used, PR), which are often isolated from patients. with some modifications. From wells that The culture media used in this study exhibited an MIC, we collected a10 L included Mueller-Hinton broth and aliquot and transferred the aliquot to Petri Sabouraud broth, which were both obtained dishes containing the appropriate culture from HIMEDIA. After growth on Petri medium for each microorganism. plates containing a suitable culture medium, the bacteria and yeasts were inoculated into After the incubation period, samples that sterile saline (0.9%) and the turbidity was showed no visible microbial growth, adjusted to McFarland standard n°0.5 to indicating the death of 99.5% of the obtain a standard concentration of microorganisms in the inoculum, were microorganisms (1 x 108colony-forming considered to have bactericidal/fungicidal unit/mL). activity. The samples with visible microbial growth were considered to have The minimum inhibitory concentration bacteriostatic/fungistatic activity. (MIC) values of the extracts and essential oil 308 Int.J.Curr.Microbiol.App.Sci (2016) 5(1): 306-317
Antioxidant Activity triplicate. These samples were incubated for 90 minutes in a 95°C water bath, and after The DPPH method that was used to cooling, the absorbance of the samples at determine the antioxidant capacity followed 695nm was measured (UV-Vis the method described by Sousa et al. (2007), spectrophotometer Shimadzu 1601, Kyoto, with some modifications. All samples (the Japan). ethyl acetate fraction, the butanol fraction, and the remaining aqueous-alcoholic raw The analytical curve was generated witha extract of both organs of the species) were 250 g/mL ascorbic acid solution using six subjected to this test at concentrations of 25 different concentrations, following the same to 250 g/mL. We used solutions of ascorbic procedure that was used for the other acid, rutin and gallic acid as positive samples. The total antioxidant capacity was controls, all at the same concentrations as determined by interpolating the average the test samples. absorbance of the samples and positive controls against the calibration curve and The analytical curve was generated with a expressed as µg of ascorbic acid/g plant DPPH solution, yielding a straight-line material (µg AA/g PM). equation (R = 0.9996), which was used for further calculations. The samples and The biological activity results were analyzed positive controls were tested in a reaction using the statistical program SISVAR mixture (0.3 ml of the sample or positive (Ferreira, 2011)and results expressed as control + 2.7 mL of the 40 g/ml DPPH mean ± standard deviation (SD) from three solution) in triplicate, and after 30 minutes, experiments. Analysis of variance was the absorbance of the samples was measured performed to detect the existence of at 515 nm using a UV-Vis differences among the factors (One way spectrophotometer (Shimadzu 1601, Kyoto, ANOVA), and the identified differences Japan). were subjected to significance comparisons using theTukey test. From the equation obtained using the calibration curve and the average DPPH Results and Discussion absorbance of each sample and positive control, it was possible to determine the Based on the obtained results (Table 1), we remaining concentration of DPPH as a can confirm that the extract from the leaves percentage, as well as the percentage of has moderate antibacterial activity antioxidant activity at all tested (Machado et al., 2005) against Salmonella concentrations. typhimurium, Escherichia coli, Enterobacter aerogenes, Proteus mirabilis, For the method in which Staphylococcus aureus, Streptococcus phosphomolybdenum complexes are pyogenes and Bacillus subtilis. However, the reduced to determine the total antioxidant antibacterial activity of this extract against capacity (Prieto et al., 1999), the same the microorganism Enteroccus faecalis was samples and positive controls were used, at low, with an MIC value of 2,000 µg/mL. the same dilutions. The reaction mixture was The effect of this extract against the eight formed by mixing 100 L of the positive bacteria used in this study was control or sample with 1 ml of the reagent bacteriostatic. solution. All reactions were performed in
309 Int.J.Curr.Microbiol.App.Sci (2016) 5(1): 306-317
Regarding the investigated yeasts (Table 2), sensitive to the action of the essential oil. this extract showed activity against only two Against C. albicans, T. beigelli and C. species: Candida glabrata, for which the tropicalis, the essential oil exhibited extract exhibited weak activity, and moderate activity. The action of the essential Trichosporon beigelli, for which the extract oil against these yeasts was fungistatic in all exhibited moderate activity. The effect of cases. this extract against both strains was fungistatic. In relation to the antioxidant capacity, the results obtained using the DPPH method The extract from the bark and stem (Table 3) revealed that all of the samples exhibited moderate antibacterial activity have antioxidant activity, with a dose- against S. typhimurium, E. coli, E. dependent profile. In addition, a significant aerogenes, S. aureus, S. pyogenes and B. difference was observed between the subtilis, with MIC values of 500 µg/mL. samples (p <0.01) and reference patterns, as However, against the strains P. mirabilis and well as between the samples tested in this E. faecalis, this extract showed weak assay. activity. Bactericidal activity of this extract was observed only against E. coli. The butanol fraction of the bark and stem showed the strongest antioxidant activity, Among the investigated yeasts, the only which was stronger than those of the species that was not sensitive to the action of reference standards that were used in this this extract was Candida krusei. The MIC study. The value displayed by the ethyl values of this extract against C. glabrata, C. acetate fraction of this same plant organ albicans, C. tropicalis and T. beigelli represented the second strongest antioxidant revealed a low activity of the extract against effect; however, the average did not differ these microorganisms. In all of these cases, from those of the ascorbic acid standard and the extract exhibited fungistatic activity. the ethyl acetate fraction of the leaves. The antioxidant activity found for the crude Analyzing the results for the essential oil extract of the leaves was statistically similar (Table 1), it can be seen that the MIC values to that exhibited by the gallic acid and rutin were low against all bacteria, except for S. standards. pyogenes. Against S. typhimurium, E. coli, E. aerogenes, S. aureus and B. subtilis, the From the results obtained using the essential oil showed MIC values of 31.25 phosphomolybdenum methodology, it can g/mL, representing good antibacterial also be seen that for both the samples and activity. Attention should be paid to the the reference patterns, the total antioxidant action of the essential oil against the bacteria capacity is dose-dependent, with the highest E. coli, S. aureus and E. aerogenes, as the concentration tested here (250 µg/mL) essential oil was capable of causing the corresponding to the highest total death of these organisms, thus confirming antioxidant capacity of all of the analyzed bactericidal activity. Concerning the other solutions. According to the statistical bacterial strains, the oil exhibited analysis (Table 4), the ethyl acetate fraction bacteriostatic activity. of the bark and stems exhibited the strongest total antioxidant capacity and was superior Regarding the investigated yeasts (Table 2), to the reference standards used (gallic acid only C. glabrata and C. krusei were not and rutin).
310
Int.J.Curr.Microbiol.App.Sci (2016) 5(1): 306-317
Table.1 Minimum Inhibitory Concentration (MIC in µg/ml) and Antimicrobial Activity of Extracts and Essential oil of Liquidambar styraciflua in Bacteria Control
Samples Microorganism Gram Oil Leaves Barkandstems Salmonella typhimurium 31,25 500 500 - ATCC 14028 Bacteriostatic Bacteriostatic Bacteriostatic Escherichia coli 31,25 250 500 - ATCC 25922 Bactericidal Bacteriostatic Bactericidal Enterobacter aerogenes 31,25 250 500 - ATCC 13048 Bactericidal Bacteriostatic Bacteriostatic Proteus mirabilis 62,5 500 1000 - ATCC 25933 Bacteriostatic Bacteriostatic Bacteriostatic Staphylococcus aureus 31,25 250 500 + ATCC 25923 Bactericidal Bacteriostatic Bacteriostatic Enterococcusfaecalis 500 2000 2000 + ATCC 29212 Bacteriostatic Bacteriostatic Bacteriostatic Streptococcus pyogenes NA 250 500 + ATCC 19615 Bacteriostatic Bacteriostatic Bacillus subtilis 31,25 500 500 + ATCC 6633 Bacteriostatic Bacteriostatic Bacteriostatic NA = No Activity
Table.2 Minimum Inhibitory Concentration (MIC in µg/ml) and Antimicrobial Activity of Extracts and Essential Oil of Liquid Ambarstyraciflua in Yeasts Control
Microorganism Samples Oil Leaves Barkandstems Candida glabrata NA 2000 2000 Fungistatic Fungistatic Candida albicans 250 NA 2000 Fungistatic Fungistatic Candida tropicalis 125 NA 2000 Fungistatic Fungistatic Candida krusei NA NA NA Trichosporon beigelli 250 250 1000 Fungistatic Fungistatic Fungistatic NA = No Activity
311
Int.J.Curr.Microbiol.App.Sci (2016) 5(1): 306-317
Table.3 Percentages of Antioxidant Activity of Samples and Positive Controls (concentration 250 µg/mL) by the DPPH method. Averages (n=3) Followed by the Same Letter do not differ by Tukey Test (p<0,01)
Samples Averages ± SD Tukey test Butanol fraction of barks and stems 104.386± 0,001 a Ethylacetate fraction of bark and stems 97.699 ± 0,001 b Ascorbic acid 96.596± 0,002 b, c Ethylacetate fraction of leaves 94.575±0,001 b, c Hydroalcoholic extract of leaves 93.955±0,001 c Gallicacid 93.544±0,001 c Rutin 93.263±0,001 c Hydroalcoholic extract of bark ands tems 82.807 ± 0,017 d Butanolfraction of leaves 77.758 ± 0,012 e Hydroalcoholic fraction of bark and stems 52.877±0,001 f Hydroalcoholic fraction of leaves 36.313± 0,037 g
Graph.1 Percentages of relative antioxidant activity of samples (EL = extract of leaves, EAL ethylacetate fraction of leaves, BL = butanol fraction of leaves, HL = hydroalcoholic fraction of leaves, EBS = extract of bark and stems, EABS = ethylacetate fracion of bark and stems, BBS = butanol fraction of bark and stems, HBS = hydroalcoholic fraction of bark and stems) and positive controls (AA = ascorbic acid, GA = gallic acid, RT = rutin) in relation to ascorbic acid by phosphomolybdenum methodology. Averages (n=3) followed by the same letter do not differ by Tukeytest(p<0,01)
312
Int.J.Curr.Microbiol.App.Sci (2016) 5(1): 306-317
Table.4 Total Antioxidant Capacity of Samples and Positive controls (concentration 250 µg/mL) by the Phosphomolydenum Method. Averages (n=3) followed by the Same Letter do not Differ by Tukey Test (p<0,01)
Samples Averages ( gAA/gPM ) ± SD Tukey test Butanol fraction of barks and stems 700.797± 0,035 a Ethylacetate fraction of bark and stems 514.710± 0,021 b Ascorbic acid 458.043± 0,013 b Ethylacetate fraction of leaves 322.101± 0,015 c Hydroalcoholic extract of leaves 283.116± 0,033 c Gallicacid 256.739± 0,010 c Rutin 187.609± 0,030 d Hydroalcoholic extract of bark ands tems 181.956± 0,015 d Butanolfraction of leaves 89.638± 0,027 e Hydroalcoholic fraction of bark and stems 71.522± 0,022 e
The butanol fraction of the bark and stem The hydroalcoholic extract of the leaves had a total antioxidant capacity similar to showed a relative percentage of antioxidant that of the gallic acid standard, while the activity similar to that of ascorbic acid, butanol fraction of the leaves exhibited a while the butanol fraction of this plant organ total antioxidant capacity similar to that of was lower than but similar to that of the the rutinstandard but lower than that of the reference standard rutin. same fraction of the bark and stem. The hydroalcoholic extracts and the ethyl acetate The antimicrobial activity observed for fraction of the leavesyielded statistically extracts of this species may be related to the equivalent results, and all of the extracts presence of polyphenols, such as flavonoids were superior to rutin but inferior to gallic and tannins, and also to the presence of acid. Through a comparison with ascorbic steroids and/or triterpenes. These classes of acid, which was considered to have 100% secondary metabolites are present in the antioxidant activity for the purposes of the hydroalcoholic extracts of both of the calculations, another comparison profile was analyzed organs (Baril, 2013), and the established between the samples and the literature contains reports of the reference standard by calculating the antimicrobial properties of these chemical percentages of relative antioxidant activity compounds (Lima, 2002). at a concentration of 250 µg/mL (Graph 1). The essential oil from the leaves of L. Analyzing these results, we found that the styraciflua showed the best antimicrobial ethyl acetate fraction of the bark and stem activity and also exhibited bactericidal was again superior to all of the samples and activity against some species, such as S. reference standards, displaying antioxidant aureus. These data are extremely valuable activity three times higher than the ascorbic because this microorganism is an important acid. The reference standard gallic acid also etiologic agent and has become a paradigm showed a higher value than ascorbic acid, of bacterial infections. S. aureus stands out along with the butanol fraction of the bark due to its high frequency and pathogenicity, and stem, and these results were statistically as well as its high versatility in acquiring similar. antimicrobial resistance, making it a
313 Int.J.Curr.Microbiol.App.Sci (2016) 5(1): 306-317 universal concern (Ferronato et al., 2007; mechanisms, such as blocking, interfering Ferreira et al., 2010). with or suppressing the activities of the enzymes involved in the generation of Approximately 64 volatile secondary reactive oxygen and nitrogen species, acting metabolites have been identified in the as chelating agents for transition metals and essential oil of L. styraciflua leaves, making them inactive, or neutralizing free including the major monoterpene radicals into stable compounds (Mosquera et hydrocarbon components d-limonene al., 2009). These characteristics of this (20.71% to 22.34%), -pinene (26.17% to group of secondary metabolites that are 27.95%) and -pinene(10.06% to 11.25%) prominent in fractions and extracts of (El- Readi et al., 2013). The antimicrobial L.styraciflua (Baril, 2013) may underlie the activity of a wide variety of essential oils is high antioxidant capacity observed in this recognized, and in most cases, this activity work. is primarily attributed to isoprenes, such as monoterpenes, sesquiterpenes and related The antioxidant activity of the essential oils alcohols, phenols and other hydrocarbons from the leaves and stem of L. styraciflua (Koroch et al., 2007), which are all was assessed by El-Readi et al. (2013) using compounds that are present in the essential three methods, including the DPPH test. oil of this species. Both essential oils had antioxidant activity, but the essential oil from the stem was more However, as the essential oil has a complex active than the essential oil from the leaf: chemical composition, its antimicrobial however, both oils exhibited weaker activity activity can likely be assigned not to a single than vitamin C. mechanism but to several mechanisms, which may result in synergistic effects or In the present study observed differences in even antagonistic effects (Silva et al., 2011). the results obtained for the L.styraciflua samples and the reference standards using The antioxidant activity results show that the the two methodologies employed in this fractions and the extract obtained from the study. This finding proves that many bark and stem of L.styraciflua exhibited complex mechanisms are used to both stronger activity than the substances used as inhibit oxidation and neutralize free radicals; references of antioxidant activity. Those therefore, the results obtained using the two fractions and extracts also exhibited higher methods should not be compared, as the values than those found for the fractions and principle of the reaction is not the same extracts of the leaves of this species. We (Malinowski, 2010). obtained the best results for antioxidant activity using the butanol and ethyl acetate Reactive oxygen species may be the fractions of both organs from L.styraciflua. principal factor involved in many The polar nature of these compounds allows degenerative diseases. For this reason, for better extraction of polyphenol antioxidants may have preventive and compounds, which have a multifunctional therapeutic effects on these diseases profile in the plant and may act as reducing (Koroch et al., 2007) and may act to reduce agents, hydrogen donors and suppressors of the development of diseases such as singlet oxygen (Koroch et al., 2007). atherosclerosis, diabetes, hypertension, and degenerative coronary and neurological Therefore, the antioxidant activity of these diseases and to reduce mutagenicity and compounds can occur through several cancer (Barbosa, 2010). 314 Int.J.Curr.Microbiol.App.Sci (2016) 5(1): 306-317
In conclusion, based on the results of this H.B.,Soares, M.J.S. andChaves, M.H., research, that the essential oil extracted from 2008. Atividade antibacteriana de the leaves of L. styraciflua exhibits plantas úteis e constituintes químicos antimicrobial activity. Emphasis should be da raiz de Coperniciaprunifera. Rev. given to the action of the essential oil Bras. Farmacogn.18: 90-97. against the bacteria E. coli, E. aerogenes and Barbosa, V.F., 2010. Caracterização do S. aureus, as the essential oil exhibited perfil da ação do ácido gálico e seus bactericidal activity against these strains. derivados sobre processos oxidativos in Therefore, natural products like the essential vitro e ex vivo.Masters dissertation, oil extracted from the leaves of L. Universidade Estadual Paulista "Julio styraciflua, are emerging as a viable way to de Mesquita Filho", Araraquara, Brazil. identify alternative treatments for these Baril, M.B., 2013. Caracterização pathogenic microorganisms. morfoanatômica e fitoquímica das partes aéreas e estudo do óleo The antioxidant capacity of the aerial parts essencial das folhas of L. styraciflua was confirmed by this Liquidambarstyraciflua, L., study, based on the stronger antioxidant Altingiaceae. Masters dissertation, activity of the extracts and fractions Universidade Federal do Paraná, obtained from the bark and stem of this Curitiba, Brazil. species. Due to the great interest in the use Chauhan, S., Jindal, M., Singh, P. of natural products, the results of this study andTewari, S., 2015. Antimicrobial have importance in determining the potential ofaqueous, methanolic beneficial effects of such products and may andethanolicextractsof Azadirachta be used as new sources of antioxidants for indica against bacterial pathogens the food industry and the pharmaceutical isolatedfromurinarytractinfectionpatient industry. s. Int.J.Curr.Microbiol.App.Sci. 4 (7): 211-214. Acknowledgement Clinical and Laboratory Standards Institute, 2005.Performance standards for The authors thank the Program of Support to antimicrobial susceptibility the Plan of Restructuring and Expansion of testing.Information supplement, 15th Federal Universities (REUNI) for granting a ed. M100-S15. Wayne. PA: scholarship, as well as all those who NCCLS/CLSI, 2005/CLSI. 2005. contributed directly or indirectly to this El-Readi, M. Z.,Eid, H.H., Ashour, M.L., work. Eid, S.Y., Labib, R.M., Sporer, F. andWink, M., 2013. Variations References ofthechemicalcompositionandbioactivit yofessentialoilsfromleavesandstemsofL Araújo, T.A.S., Alencar, N.L., Amorim, iquidambarstyraci ua (Altingiaceae). E.L.C. andAlbuquerque, U.P., 2008.A J.Pharm.Pharmacol. 65 (11): 1653- new approach to study medicinal plants 1663. with tannins and flavonoids contents Ferreira,D.F., 2011.Sisvar: a computer from the local knowledge.J. statistical analysis system. Ethnopharmacol. 120: 72-80. Cienc.Agrotecnol.35 (6): 1039-1042. Ayres, M.C.C., Brandão, M.S.,Vieira- Ferreira, S.B.,Palmeira, J.D., Souza, J.H., Júnior, G.M., Menor,J.C.A.S.,Silva, Almeida, J.M., Figueiredo, M.C.P.,
315 Int.J.Curr.Microbiol.App.Sci (2016) 5(1): 306-317
Pequeno, A.S., Arruda, T.A., Antunes, Liquidambar formosana fruits. Planta R.M.P. & Cand Ramalho, R.M., 2010. Med. 54: 417 419. Avaliação da Atividade Antimicrobiana Koroch, A.R.,Juliani, H.R. and Zygadlo, in vitro do extrato hidroalcóolico de J.A., 2007. Bioactivity of Essential Oils Stryphnodendro nadstringens (Mart.) and Their Components. In: Berger, Coville sobre isolados ambulatoriais de R.G. (Ed.), Flavours and Fragrances: Staphylococcus aureus. Rev. Bras. Chemistry, Bioprocessing and Anal. Clin.42 (1): 27-31. Sustainability.Springer, Berlim,pp. 87- Ferronatto, R.,Marchesan, E.D.,Pezenti, 117. E.,Bednarski, F. and Onofre, S.B., Lee, Y-S., Kim, J., Lee, S-G., Oh, E., Shin, 2007. Atividade antimicrobiana de S-C. and Park, I-K., 2009.Effects of óleos essenciais produzidos por plant essential oils and components Baccharis dracunculifolia D.C. e from oriental sweet gum (Liquidambar Baccharis uncinella D.C. (Asteraceae). orientalis) on growth and Rev. Bras. Farmacogn.17 (2): 224-230. morphogenesis of three Hanamanthagouda, M.S., Kakkalameli, phytopathogenic fungi. Pestic. S.B.,Naik, P.M.,Nagella, P.,S Biochem. Physiol.93: 138 143. eetharamareddy, H.R. and Murthy, Lima, E.O., 2002. Plantas e suas H.N., 2010.Essential oils of Lavandula propriedades antimicrobianas: uma bipinnata and their antimicrobial breve análise histórica. In: Yunes, R.A. activities. Food Chem.118: 836-839. andCalixto, J.B. (Eds.), Plantas Ickert-Bond, S.M.,Pigg, K.B. andWen, J., Medicinais sob a ótica da Química 2005.Comparative infructescence Medicinal Moderna. morphology in Liquidambar Argos,Chapecó,pp.481-501. (Altingiaceae) and its evolutionary Lingbeck, J.M.,O`Bryan, C.A., Martin, significance. Am. J. Bot.92: 1234- E.M., Adams, J.P. andCrandall, P.G., 1255. 2015. Sweetgum: anancientsourceof Ickert-Bond, S.M.,Wen, J., 2006. Phylogeny beneficial compounds with modern and biogeography of Altingiaceae: benefits. Pharmacogn. Rev. 9 (17): 1- Evidence from combined analysis of 11. five non-coding chloroplast regions. Lorenzi, H.,Souza, H.M., Torres, M.A.V. Mol. Phylogenet. Evol.39: 512-528. andBacher, L.B., 2003. Árvores Kim,J.,Seo, S., Lee, S.,Shin, S.andPark, I., exóticas no Brasil: madeireiras, 2008.Nematicidalactivityofplantessenti ornamentais e aromáticas, 1st ed. aloilsandcomponentsfromcoriander Instituto Plantarium de Estudos da (Coriandrum sativum), oriental Flora, Nova Odessa, SP. sweetgum (Liquidambar orientalis), Machado, M., Cechinel Filho, V., Tessarolo, andvalerian (Valeriana wallichii) R.,Mallmann, R., Silva, C.M. and Cruz, essential oils against pine wood A.B., 2005. Potent antibacterial activity nematode (Bursaphelen of Eugenia umbelliflora. Pharm. Biol. chusxylophilus). J. Agric. Food Chem. (London, U. K.)43 (7): 636-639. 56: 7316 7320. Mosquera, O. M., Correra, Y.M. andNiño, Konno, C., Oshima, Y.,Hikino, H., Yang, J., 2009. Antioxidant activity of plant L.L. andYen, K.Y., 1988. extracts from Colombian flora. Rev. Antihepatotoxic principles of Bras. Farmacogn.19 (2A): 382-387. Malinowski, L.R.L., 2010.Morfoanatomia,
316
Int.J.Curr.Microbiol.App.Sci (2016) 5(1): 306-317
Fitoquímica e Atividades Biológicas de Pharmaceuticals4 (12): 1535-1550. folhas jovens de Eucalyptusglobulus Silver, L.L. andBostian, K.A., Labill. subespéciebicostata (Maiden et 1993.Discovery and development of al.) J. B. Kirkpat., Myrtaceae.Masters new antibiotics: The problem of dissertation, Universidade Federal do antibiotic resistance. Antimicrob. Paraná, Curitiba, Brazil. Agents Chemother.37: 377-383. Prieto, P., Pineda, M. and Aguilar, M., Sousa, C.M.M.,Rocha e Silva, H.,Vieira- 1999.Spectrosphotometric quantitation Jr.,G.M., Ayres, M.C.C.,Da Costa, of antioxidant capacity through the C.L.S.,Araújo, D.S.,Cavalcante, formation of a phosphomolybdenum L.C.D.,Barros, E.D.S.,Araújo, complex: specific application to the P.B.M.,Brandão, M.S.andChaves, determination of vitamin E.Anal. M.H., 2007.Fenóis totais e atividade Biochem.269: 337-341. antioxidante de cinco plantas Sadi, G., Emsen, B., Kaya, A., Kocabas, A., medicinais. Quim. Nova30 (2): 351- Çinar, S.andKartal, D.I., 2015. 355. Cytotoxicityof some edible mushrooms Veljic, M., Ciric, A.,Sokovic, extracts over liverhepatocellular M.,Janackovic, P. and Marin, P.D., carcinoma cells in conjunction with 2010. Antibacterial and antifungal their antioxidant and antibacterial activity of the liverwort properties. Pharmacogn. Mag.11 (Ptilidiumpulcherrimum) methanol (S1):6-18. extract.Arch. Biol. Sci. (Engl. Sa diç, O.,Ozkan, G., Ozcan, Transl.)62 (2): 381-385. M.andOzçelik, S.,2005. A study Yang,N-Y., Chen, J-H.,Zhou, G-S., Tang, oninhibitoryeffectsof sigla tree Y-P., Duan, J-A., Tian, L-J. and Liu, (Liquidambar orientalisMill. var. X-H., 2011. Pentacyclictriterpenes orientalis) storaxagainstseveralbacteria. from there in of Liquidambar Phytother Res. 19: 549 551. formosana. Fitoterapia 82: 927 931. Silva, S.M., Abe, S.Y.,Murakami, Wang, K., Pan, Y., Wang, H., Zhang, Y., F.S.,Frensch, G.,Marques, F.A. Lei, Q.,Zhu, Z., Li, H. andLiang, andNakashima, T., 2011. Essential Oils M.,2010. Antioxidant activitiesof from Different Plant Parts of Liquidambar formosana Hanceleaf Eucalyptus cinerea F. Muell. exBenth. extracts. Med. Chem. Res. 19: 166 (Myrtaceae) as a Source of 1,8-Cineole 176. and Their Bioactivities.
How to cite this article:
Graziele Francine Franco Mancarz, Ana Carolina Pareja Lobo, Mariah Brandalise Baril, Francisco de Assis Franco and Tomoe Nakashima. 2016. Antimicrobial and Antioxidant Activity of the Leaves, Bark and Stems of Liquidambar styraciflua L. (Altingiaceae). Int.J.Curr.Microbiol.App.Sci. 5(1): 306-317. http://dx.doi.org/10.20546/ijcmas.2016.501.029
317