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Phytochemical and Biological Properties of Ferulasharifi Essential OilRazzagh Mahmoudia, Morteza Kosarib & Shiva Baratica Department of Food Hygiene and Aquatics, Faculty of Veterinary Medicine, University ofTabriz, Tabriz, Iranb Laboratory of Plant Biotechnology, Hayyan Research Center, University of Tabriz, Tabriz,Iranc Faculty of Agriculture, University of Tabriz, Tabriz, IranPublished online: 23 Dec 2013.

To cite this article: Razzagh Mahmoudi, Morteza Kosari & Shiva Barati (2013) Phytochemical and BiologicalProperties of Ferula sharifi Essential Oil, Journal of Biologically Active Products from Nature, 3:5-6, 331-338, DOI:10.1080/22311866.2013.867664

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Phytochemical and Biological Properties of Ferula sharifi Essential Oil

Razzagh Mahmoudi 1*, Morteza Kosari 2 and Shiva Barati 3

1 Department of Food Hygiene and Aquatics,Faculty of Veterinary Medicine, University of Tabriz, Tabriz, Iran

2 Laboratory of Plant Biotechnology, Hayyan Research Center,University of Tabriz, Tabriz, Iran

3 Faculty of Agriculture, University of Tabriz, Tabriz, Iran

Abstract: This study presents the phytochemical components and antibacterial properties of thehydrodistilled essential oil (EO) of Ferula sharifi. The EO components were identified by GC-MS analysis.The minimum inhibitory concentration (MIC) and mininmum bactericidal (MBC) of EO against four selectedprobiotic microorganisms (Lactobacillus casei, Lactobacillus acidophilus, Lactobacillus plantarum andLactobacillus ramnus) was determined using micro-plate assay. Thirty components representing 96.9 % of thetotal oil were characterized. The main chemical group was monoterpene hydrocarbons (43.9 %) including β-pinene (21.7 %), α-pinene (15.9 %) and sabinene (5.7 %). The MIC and MBC values ranged between 1250-10000 ppm., L. acidophillus was the susceptible (MIC: 1250 ppm and MBC: 5000 ppm) among the testedmicroorganism. Our results showing that the genus Ferula is considered as a good source of EO and antibacterialactivity against probiotic bacteria. So its use as natural additives in functional foods need to be furtherinvestigated.

Key words: Essential oil, Ferula sharifi, GC/MS, Probiotic.

IntroductionIncreased public awareness of the negative

effects caused by over exposure to syntheticchemicals has led to the search for green solutionslike medicinal plants 1,2. Even today, plantmaterials continue to play a major role in primaryhealth care as therapeutic remedies in manydeveloping countries 3. Medicinal herbs containphysiologically active principles that over theyears have been exploited in traditional medicinefor the treatment of various ailments as theycontain anti-microbial properties 4,5. The genusFerula, belonging to the family Apiaceae,comprises about 170 species. These are producedfrom central Asia westward to northern Africa.

The Iranian flora comprises of 30 species ofFerula, of which some are endemic. The popularPersian name of the most species is “Koma” 6.The chemistry of this genus has been studied bymany investigators. To date, more than 70 speciesof Ferula have been investigated chemically 7,8.The plants of this genus are well documented asa good source of biologically active compoundssuch as Sesquiterpenoids and sulfur containingcompounds 6. Several species of this genus havebeen used in traditional medicine for thetreatment of various organ disorders. Amongdifferent Ferula species that have been used asnatural remedies, F. assa-foetida used asanticonvulsant, carminative, antispasmodic,

*Corresponding author (Razzagh Mahmoudi)E-mail: < Mahmodi@tabrizu.ac.ir > © 2013, Har Krishan Bhalla & Sons

ISSN Print: 2231-1866ISSN Online: 2231-1874

TBAP 3 (5 & 6) 2013 pp 331 - 338 331

Received 14 July 2013; accepted in revised form 13 August 2013

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diuretic, aphrodisiac, antihelmintic, tonic, andlaxative, alterative, F. badrakema and F.gummosa both used as anti-convulsant, tonic,anti-hysteric, decongestant, treatment of neuro-logical disorders, and stomachache, and F. persicaused as laxative, carminative, antihysteric,treatment of lumbago, diabetes, rheumatism, andbackache are most famous 9,6. Antimicrobialproperties of herbs have been documented inancient literature and the interest continues to thepresent. Spices are herbal products which havebeen safely used by people around the world toimpart desirable flavors and aromas to the localfoods. It looks that there has been a naturalselection for spices as these products are mainlyoriginated from plants grown in the tropicalregions with wide distribution of food-bornebacteria. Several of these spices and their EOshave been reported to posses antimicrobialactivities including garlic, savory, basil, laurel,mint, cumin, onion, sumac, menthe, allium,Pimpinella and thyme 10,11,12,13,14.

Despite extensive studies on the antimicrobialeffects of EOs against pathogenic bacteria, fewstudies on effect of this component against oflactic acid bacteria activity especially probioticsbacteria has been reported. Thus we decided toinvestigate the chemical composition and effec-tiveness of the EO isolated from Ferula sharifion some probiotic bacteria.

Material and methodsPlant material

The seeds of F. sharifi were collected on May2012 from Jeylun mountain which is located inCharmahal Bakhtiari province (south western ofIran). The plant identity was confirmed byherbarium of the faculty of Pharmacy, Universityof Tabriz, Tabriz, Iran under code number (722Tbz-Fph).

Extraction and isolation of the EOEO was obtained by hydro distillation of 100 g

of dried seeds using a Clevenger-type apparatusfor 3 h. Diethyl ether (10 mL) was used as thecollector solvent. After evaporation of the solvent,the oil was dried over anhydrous sodium sulfateand stored in sealed vials protected from the light

at -20°C before analyses 15.

GC AnalysisThe EO was analyzed by gas chromatography

(GC) (Agilent 6890, USA). The chromatographwas equipped with HP-5MS capillary column (30× 0.2 mm ID × 0.2 μm film thickness) and thedata were acquired under the followingconditions: initial temperature 50°C; program rate15°C min-1; final temperature 300°C (holding for20 min) and injector temperature 290°C. Thecarrier gas was Helium and the split ratio was0.8 ml min-1 16.

GC-MS AnalysisThe EO was also analyzed by gas chromato-

graphy mass spectrometry (GC-MS) (Agilent6890 gas chromatography equipped with Agilent5973 mass selective detector, USA) and the samecapillary column and analytical conditionsindicated above. The MS was run in the electronionization mode, using ionization energy of 70eV (Fig.1) 16.

Bacterial strainThe EO was individually tested against four

probiotic bacteria. Commercial lyophilizedcultures of the probiotic Lactobacillus caseiATCC3939, Lactobacillus acidophilusATCC4356, Lactobacillus plantarum ATCC 4142and Lactobacillus ramnus ATCC 5031 wereobtained from the Iranian Organization of Indus-trial Research. Sub cultivation and preparationof the probiotic bacteria were conducted accor-ding to standard method 17.

Antimicrobial activityMicro-well dilution assay

The minimal inhibition concentration (MIC)and minimal bactericidal concentration (MBC)values were studied for the bacterial strains inmicro plate. The inocula of the bacterial strainswere prepared from 12 h MRS1 broth culturesand suspensions were adjusted to 0.5 McFarlandstandard turbidity. EO dissolved in 10 %dimethylsulfoxide (DMSO) were first diluted tothe highest concentration (10000 ppm) to betested, and then serial two-fold dilutions were

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made in a concentration range 10000-625 ppmin 10 ml sterile test tubes containing MRS broth.MIC values of EO against probiotic bacteriastrains were determined based on a micro-welldilution method. The 96-well plates wereprepared by dispensing into each well 95 μl ofMRS broth and 5 μl of the inoculums. A 100 ppmaliquot from the stock solution of EO initiallyprepared at the concentration of 10000 ppm wasadded into the first wells. Then, 100 ppm fromtheir serial dilutions was transferred into 5consecutive wells. The last well containing 195μl of MRS broth without compound and 5 ppmof the inoculums on each strip was used as thenegative control. The final volume in each wellwas 200 ppm. The plates were covered with asterile plate sealer. Contents of each well weremixed on plate shaker at 300 rpm for 20s andthen incubated at appropriate temperatures for24h. Microbial growth was determined byabsorbance at 600 nm using the EL _800universal micro plate reader (Biotek Instrumentinc, Highland Park, Vermont, USA) andconfirmed by plating 5 μl samples from clearwells on nutrient agar medium. These EO testedin this study were screened two times againsteach organism. The MIC and MBC were definedas the lowest concentration of the compounds to

inhibit the growth of microorganisms and bacteri-cidal effects on microorganisms respectively 18.

Statistical analysisStatistical analysis was performed using SPSS

17, all the tests were conducted in triplicate, andthe data obtained were analyzed by Analysis ofVariance (ANOVA). The Statistical significancewas determined at P<0.05.

Results and discussionThis study focused essentially on the phyto-

chemical and antibacterial screening of F. sharifiEO. Table 1 shows the results of GC-MS analysisof the F. sharifi EO. The compounds are listed inorder of their retention time. A total of 30components have been identified in the oil,representing 96.9 % of the total oil. The maingroup was monoterpene hydrocarbons (43.4 %)including β-pinene (21.7 %), α-pinene (15.9 %)and sabinene (5.7 %). the other main componentswere found to be naphthalene (7.9 %), isolongifol(6.7 %), trans-pinocarveol (5.1 %), myrtenol (4.8%), azulene (3.8 %).

The yield was 1.60 % on dry weight basis. TheEO obtained from the roots of F. ferulaoidesyielded 2.4-3.2 % of EO from dry roots 20 andaverage 1.7 %-3.8 % in the fruits of F. gummosa

Figure 1. Chromatogram of F. sharifi Essential Oil

GC-MS Chromatogramintensity

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19. Concerning the chemical composition of theEO of other Ferula species, Shatar 20 showed thatthe roots of F. ferulaoides growing in Mongoliawere dominated by guaiol (58.8 %), and (E)-nerolidol (10.2 %). In the fruits of F. gummosafrom Iran, the major components were β-pinene(43.8 %), α-pinene (27.3 %) 21, also found β-pinene (43.8 %), α-pinene (27.8 %) of F.gummosa growing in Isfahan 19, also reported thatthe essential oil of the F. latisecta collected inIran was characterized by high contents of Z-

ocimenone (32.4 %), E-ocimenone (20.3 %), andcis-pinocarvone (11.4 %) 19. Different quantitiesof the same component such as β-pinene (82.0%), α-pinene (5.4 %) and myrcene (3.4 %) werereported in fruit essential oil of F. gummosacollected from Tehran 22. Its appears oxygenatedmonoterpenes components such as α-pinene, β-pinene, camphene and sabinene were the majorfraction of the oils of Ferula speciecs 23. Ourresults also showed that these compounds werethe main components of F. sharifi (Table 1).

Table 1. Constituents of F. sharifi Essential Oil by GC-MS

No. Compunds RT* (%)

1 α-Pipene 13.2 15.92 Camphonen 13.8 0.73 Sabinene 14.8 5.74 β-Pinene 15.1 21.75 β-Myrcene 15.4 0.66 Carene 16.6 2.17 p-Cymene 16.9 0.78 Limonene 17.3 0.69 trans-Pinocarveol 22.5 5.1

10 Benzene 24.1 1.811 p-Cymenen 24.3 1.412 Norpinene-2-carboxaldehyde, 6,6-dimethyl 24.8 2.213 Myrtenol 25.3 4.814 β-Terpinyl acetate Cyclohexanol 32.7 1.015 Sesquiphellandrene 36.6 1.116 β-Caryolhyllene 36.8 0.117 Germacrene D 37.2 0.118 Azulene 37.9 3.819 α-Humulene 38.2 0.520 Naphthalene 39.1 7.921 β-Chamigrene 39.3 0.922 Germacrene B 40.1 0.823 Isolongifol 40.3 6.724 Cyclohexene 40.4 1.025 Spathulenol 40.9 1.326 δ-Cadinene 41.0 0.427 Caryophyllene oxide 41.3 0.928 Nerolidol B 42.4 2.729 Guaiol 44.1 2.830 Cubenol 45.7 1.7

Total 96.9

*Retention time (min)

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Antimicrobial activityThe growth inhibition value of EO on microbial

strains is shown in table 2. The results showedsignificant differences (P<0.05) was found in thesusceptibility of Lactobacillus acidophillus toantimicrobial activity of this essential oilcompared to other bacteria (Fig. 2), among theprobiotic bacteria tested, L. acidophillus showedthe susceptible bacteria (MIC:1250 ppm, MBC:5000 ppm) to the antibacterial activity of the F.sharifi EO (Table 2).

Figure 3. Effect of F. sharifi EO on growth probiotic bacteria bydilution assay (A-E: EO serial dilution: 10000, 5000, 2500, 1250, 625 ppm.

F: culture without EO and probiotic bacteria, G: bacteria without EO and H: EOwithout bacteria, L1: L. acidophillus, L2: L. casei, L3: L. plantarum and L4: L. ramnus).

Table 2. Antibacterial activity (MIC and MB) of F. sharifi Essential Oil

Microorganisms MIC (ppm) MBC (ppm)

Lactobacillus acidophilus 1250 5000Lactobacillus casei 5000 10000Lactobacillus ramnus 5000 10000Lactobacillus plantarum 5000 NE

NE: Not effect

Antibacterial properties EO of many speciesof ferula against pathogenic microorganismreported by researchers, The EO from the fruitsof F. badrakema was found to be moderatelyactive against Staphylococcus aureus andBacillus cereus as Gram-positive bacteria, andCandida albicans as fungal strain. However,Gram-negative bacteria (Escherichia coli andPseudomonas aeruginosa) appeared not to besusceptible to inhibitory effects of this EO 24.

In another study, the EO from F. glauca was

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evaluated for antibacterial and antifungal activity.The results showed that the Gram-positive B.subtilis was the most sensitive strain. The EOsalso showed moderate inhibitory activity againstStrptococcus mutans, Enterococcus faecalis andE. coli whereas no remarkable activity wasobserved against S. aureus and the yeast C.albicans (which was the most resistant strain).Findings also demonstrated that leaves and fruitsessential oils were the most active oils of the planton the tested microorganisms 24. Concerning theF. latisecta, the polysuphide-rich fruit oil of thisplant was shown to possess antibacterial activityagainst Gram-positive (B. cereus and in particularS. aureus) but not Gram-negative bacteria (P.aeruginosa and E. coli) and a relatively potentinhibitory activity against C. albicans 7.

Moreover, this oil was tested for its antifungalactivity against a range of human pathogenicdermatophytes (Trichophyton mentagrophytes, T.rubrum, T. verrucosom, Microsporum canis andM. gypseum). The results showed that the oil wasactive against all tested dermatophytes with themost significant activity against T. rubrum andT. verrucosom 7. In another study, the essentialoil from the aerial parts of F. latisecta wasreported to exert high inhibitory activity againstthe Gram-positives B. subtilis and E. faecalis,moderate activity against S. aureus, E. coli andKlebsiella pneumoniae and was inactive againstP. aeruginosa 26.Concerning the F. gummosa, itwas found that the essential oil from the fruits ofthe plant possesses strong antibacterial andantifungal activities against Gram-positive (S.aureus, S. epidermis and B. subtilis) and negative(E. coli, Salmonella typhi and Pseudomonasaeruginosa) bacteria and fungi (C. albicans andC. kefyr) 21.

EOs from plants and bacteriocins fromprobiotic bacteria (especially various species ofLactobacillus) have well-known antimicrobialeffects which can substitute chemicalpreservatives to control and prevent the activityof foodborne pathogens. Besides, they exertpositive effects on consumer’s health 27. Someresearch has shown the effect of plant-derivedvolatile oils on growth and viability of some lacticacid bacteria 28. Kivanc et al. 28 also showed that

EOs of Mentha longifolia and Cuminum cyminumin low concentrations lead to stimulation ofgrowth and acid production; in high concen-trations, they prevented L. plantarum growth. Ina study conducted by Simsek et al 29, EOs ofspearmint, thyme and garlic had no inhibitoryeffects on growth and durability of lactic acidbacteria present in Ayran.

Zaika and Kissinger 30 showed that M.longifolia EO can motivate, delay or preventlactic acid bacteria according to application case.Different concentrations of herbal essential oilscan influence the activity of starter bacteria infermentative dairy products 30, 32.

The results of our previous study (Effects ofMentha longifolia L. EO on viability and cellularultrastructure of L. casei during ripening ofprobiotic Feta cheese) indicated that even thehighest concentration of this essential oil casedthe highest viability of L. casei and the lowest pHvalue compared with other treatments (P< 0.05).Electron microscopy showed that essential oil wasnot harmful effect on L. casei cell membrane 32.

The GC-MS analysis showed that the majorconstituents of the EO examined in our studywere monoterpene hydrocarbons. The anti-microbial activity of the oil may be associatedwith the relatively high α-pinene (15.9 %) andβ-pinene (21.7 %) content. It has been reportedthat these components have significantantimicrobial activities 33. Antibacterial activitiesof α-thujene, 3-carene and terpinene-4-ol againstE. coli, P. aeruginosa and S. aureus have alsobeen reported 34. The bacteriostatic properties ofthe oil are suspected to be associated with thehigh α-pinene and β-pinene content, which hasbeen tested previously and was found to have asignificant antibacterial activity 34.

Among Gram-positive bacteria, lactic acidbacteria are often known as the most resistantspecies against antimicrobial agents of herbs 28.While our finding (Fig.2) showed the F. sharifiEO relatively high antibacterial activity againstall tested probiotic bacteria.

ConclusionThe results presented here can be considered

as the first information on the phytochemical and

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antimicrobial properties of F. sharifi EO. Thereare numerous benefits of probiotics and herbalessential oils, and therefore, the use of thesebacteria or bacteriocins purified from them incombination with herbal extracts and EOs asbiological preservatives may revolutionize thefood industry. Our study of the Iranian F. sharifiseeds led to the extraction and characterizationof 30 compounds followed by the evaluation of

antimicrobial activity against probiotic bacteriafor the first time. The beneficial effects ofprobiotic bacteria and spices in improved qualityand sensory characteristics of food, is necessaryto assessment of the application of F. sahrifi EOin functional foods, also phytochemical studieswill be necessary to isolate the active constituentsand evaluate the antibacterial activities against awide range of bacteria population.

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2014