antibacterial and antioxidant properties of ailanthus altissima swingle leave extract to reduce...

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ANTIBACTERIAL AND ANTIOXIDANT PROPERTIES OFAILANTHUS ALTISSIMA SWINGLE LEAVE EXTRACT TO

REDUCE FOODBORNE PATHOGENS AND SPOILING BACTERIA

ATIQUR RAHMAN1,2, EUN LYANG KIM1 and SUN CHUL KANG1,3

1Department of BiotechnologyDaegu University

Kyoungsan, Kyoungbook 712-714, Korea

2Department of Applied Chemistry and Chemical TechnologyIslamic University

Kushtia, Bangladesh

Accepted for Publication April 19, 2008

ABSTRACT

The antibacterial and antioxidant potentials of methanolic extracts ofAilanthus altissima Swingle leaves were evaluated. Antibacterial activity wastested in vitro by agar disk diffusion method against 11 (six gram-positive andfive gram-negative) foodborne bacteria. The methanol extract and its differentpolar subfractions inhibited significantly the growth of all six gram-positivebacteria: Listeria monocytogenes (ATCC 19116, ATCC 19118 and ATCC19166), Staphylococcus aureus (ATCC 6538 and KCTC 1916) and Bacillussubtilis ATCC 6633 and two gram-negative bacteria: Pseudomonas aerugi-nosa KCTC 2004 and Escherichia coli ATCC 8739. The zones of inhibition ofmethanol extract and its derived different polar subfractions against the testedbacteria were found in the 12.1–23.2 mm range and the minimum inhibitoryconcentration values were recorded between 62.5 and 500 mg/mL. Antioxidantactivity was evaluated by using 1,1-diphenyl-2-picrylhydrazyl assay. The freeradical scavenging activity of ethyl acetate (EtOAc) fraction was superior toall other fractions (IC50 = 16.45 mg/mL) and was higher than synthetic anti-oxidant butylated hydroxyanisole (IC50 = 18.27 mg/mL). Furthermore, theamount of total phenolic compounds was determined and its content inEtOAc fraction (12.25%) was the highest compared with other extract orfractions.

3 Corresponding author. TEL: +82-53-850-6553; FAX: +82-53-850-6559; EMAIL: [email protected]

DOI: 10.1111/j.1745-4565.2009.00172.x

Journal of Food Safety 29 (2009) 499–510.© 2009, Wiley Periodicals, Inc. 499

PRACTICAL APPLICATIONS

The natural products derived from Ailanthus altissima Swingle maycontribute to the development of new antimicrobial agents with potentialapplications in food industries as natural preservatives or flavoring agents tocontrol foodborne pathogens. They can be used as growth inhibitors of Listeriamonocytogenes, Staphylococcus aureus, Bacillus subtilis, Escherichia coli andPseudomonas aeruginosa, as well as some important foodborne pathogens andspoiling bacteria. The main reason for their suitability is their natural origin,which consumers find comforting and is beneficial for the environment, andthe very low risk that pathogens will develop resistance to the mixture ofcomponents that make up the extracts with their apparent diversity of antibac-terial mechanisms. These beneficial characteristics could increase food safetyand shelf life.

INTRODUCTION

Foodborne illnesses caused by the consumption of contaminated foodsare still a major problem in the world, even in well-developed countries (Meadet al. 1999). Microorganisms such as Listeria monocytogenes, Staphylococcusaureus, Bacillus subtilis, Escherichia coli, Salmonella sp. and Pseudomonasaeruginosa are the foodborne pathogens most responsible for food contami-nation (Deak and Beuchat 1996; McCabe-Sellers and Samuel 2004). Rawand/or processed foods are open to contamination during the production, saleand distribution of the foods (Deak and Beuchat 1996). A variety of differentchemicals and synthetic compounds have been used as antimicrobial agents toinhibit bacteria in foods. Due to the identified and potential toxicity of chemi-cal food preservatives and a growing concern of microbial resistance towardconventional preservatives, there has been an increased attention on naturallyderived compounds, such as plant extracts, as antimicrobial agents in foods(Schuenzel and Harrison 2002; Nasar-Abbas and Halkman 2004).

Also, there is a growing interest in research on food components such asphenolic compounds because of their possible linkage to health benefits, e.g.,reduction of heart disease and cancer, based on their antioxidant activity(Seeram et al. 2002). Many medicinal plants contain a large amount of anti-oxidants such as polyphenols, which have an important role in preventingaging and a variety of stress-related diseases because these are closely relatedto the active oxygen and lipid peroxidation (Noguchi and Niki 1999).However, there have been concerns about synthetic antioxidants such as buty-lated hydroxyanisole (BHA) and butylated hydroxytoluene because of theirpossible activity as promoters of carcinogenesis (Barlow 1990). Consequently,

500 A. RAHMAN, E.L. KIM and S.C. KANG

there is a scientific interest to find naturally occurring antioxidants for use asnatural preservative ingredients in foods or medicinal materials to replacesynthetic antioxidants, which are being restricted because of their carcinoge-nicity (Velioglu et al. 1998).

Ailanthus altissima Swingle, commonly known as the “tree of heaven,” isused in traditional medicine in many parts of Asia, including China, Japan andKorea to treat cold and gastric diseases and as an antitumor agent. Previousphytochemical studies have demonstrated the presence of quassinoids (Kubotaet al. 1996) as well as indole and b-carboline alkaloids in this plant (Ohmotoand Koike 1984; Souleles and Kokkalou 1989). Quassinoids are reported fortheir various biological activities such as antitumor, antimalarial, insecticidaland anti-inflammatory effects (Okano et al. 1990). Indole and b-carbolinealkaloids have shown inhibitory activity of cyclic adenosine monophosphate(cAMP) phosphodiesterase (Ohmoto et al. 1988).

Extracts of the plant leaves have demonstrated antiproliferative (De Feoet al. 2005), central nervous depressant (Crespi-Perellino et al. 1988), anti-feedant and insecticide (Kraus et al. 1994) activities. Fruit extracts of A.altissima Swingle occurring in China have shown antibacterial properties(Zhao et al. 2005). However, the antibacterial activity of the leave extractsof A. altissima Swingle against foodborne pathogenic bacteria as well as itsantioxidant property has not been reported. Hence, it is aimed to investigate theantibacterial and antioxidant properties of A. altissima Swingle leave extractsto inhibit the growth of foodborne pathogens and spoiling bacteria. The resultof this study differed from the result of the previous report. In general, thebiological activities alter because of changes in the chemical compositions ofplant products from several differences (origin, species, climate, and extrac-tion and analysis methods).

MATERIALS AND METHODS

Plant Material

Leaves of A. altissima Swingle (Simaroubaceae) were collected fromKyungsan city in South Korea in July 2006 and were identified by ProfessorKi Hwan Bae. A voucher specimen (CNU 923) has been deposited in theherbarium of the College of Pharmacy, Chungnam National University, SouthKorea.

Preparation of Crude Methanolic Extracts

The dried leaves of A. altissima Swingle were extracted with methanol(MeOH). The MeOH (6.52%, w/w) extract was then suspended in water and

501ANTIBACTERIAL ACTIVITY OF AILANTHUS ALTISSIMA

partitioned successively with n-hexane, chloroform (CHCl3), ethyl acetate(EtOAc) and butanol (BuOH) to yield hexane (1.89%, w/w), CHCl3 (1.14%,w/w), EtOAc (0.72%, w/w) and BuOH (1.07%, w/w) subfractions separately.Solvents (analytical grade) for extraction were obtained from commercialsources.

Microorganisms

A total of 11 foodborne pathogens and spoiling bacteria, including threestrains of L. monocytogenes ATCC 19116, 19118 and 19166; two strains of S.aureus ATCC 6538 and KCTC 1916; two strains of E. coli 0157:H7 ATCC43888 and ATCC 8739; and one strain each of B. subtilis ATCC 6633, P.aeruginosa KCTC 2004, Salmonella typhimurium KCTC 2515 and Salmo-nella enteritidis KCTC 12021, were used in this study. The strains wereobtained from the Korea Food and Drug Administration, Daegu, South Korea.L. monocytogenes strains were maintained on Brain–Heart Infusion agar(Bacto, Rockville, MD) medium at 4C. The other strains were maintained onLuria Broth agar medium (Acumedia Manufacturers, Inc., Lansing, MI) at 4C.

Antibacterial Activity Assay

The agar diffusion method (Murray et al. 1995) was used for antibacterialassay. Whatman No. 1 sterile filter paper disks (6 mm in diameter) (WhatmanInternational Ltd., Madstone, England) were impregnated with 10 mL of50 mg/mL (0.5 mg/disk) plant extracts and placed on the inoculated agar.Negative controls were prepared using the same solvent employed to dissolvethe samples. Standard reference antibiotics, tetracycline and streptomycin(10 mg/disk, each from Sigma Aldrich Co., St. Louis, MO) were used aspositive controls for the tested bacteria. Antibacterial activity was evaluated bymeasuring the diameter of the zones of inhibition against the tested bacteria.Each assay in this experiment was replicated three times.

Minimum Inhibitory Concentration (MIC)

MIC of the MeOH extract and subfractions of MeOH extract from A.altissima Swingle leaves was tested by a twofold serial dilution method (Chan-drasekaran and Venkatesalu 2004). The lowest concentration of the testsamples that did not show any growth of tested organism after macroscopicevaluation was determined as the MIC.

Antioxidant Assay

The antioxidant activity of the MeOH extract and its various subfractionsfrom leaves of A. altissima Swingle was measured on the basis of the


scavenging activities of the stable 1,1-diphenyl-2-picrylhydrazyl (DPPH) freeradical (Cuendet et al. 1997). IC50 values (concentration of sample required toscavenge 50% of free radicals) were calculated from the regression equation,prepared from the concentration of the extract or fractions, and percentageinhibition of free radical formation/percentage inhibition DPPH was assayed.Synthetic antioxidant reagents, BHA and l-ascorbic acid, were used as posi-tive controls, and all tests were carried out in triplicate.

Determination of Total Phenolics

Total phenolic constituents of the aforementioned extracts were deter-mined by a Folin–Ciocalteu reagent in alkaline medium (Lister and Wilson2001) and was expressed as gallic acid equivalents (GAE). The absorbance ofsamples was measured at 760 nm, and the results were expressed in milligramsof gallic acid/g (GAE) of dry weight of samples.

RESULTS AND DISCUSSION

The results of antibacterial activity of MeOH extract and its varioussubfractions of A. altissima Swingle against foodborne pathogens and spoilingbacteria are shown in Table 1. Results showed that the plant extracts hadremarkable activity against most of the organisms tested. In particular, theplant extracts inhibited the growth of all six gram-positive bacteria: L. mono-cytogenes (ATCC 19116, ATCC 19118 and ATCC 19166); S. aureus (ATCC6538 and KCTC 1916) and B. subtilis ATCC 6633; and two gram-negativebacteria, P. aeruginosa KCTC 2004 and E. coli ATCC 8739. MeOH extractand its polar subfractions (EtOAc and BuOH) exhibited a potent antibacterialactivity against the bacteria tested, with diameter zones of inhibition in the12.1–23.2 mm range, as shown in Table 1. Chloroform fraction also inhibitedmoderately the growth of some organisms. However, hexane fraction did notshow any activity (data not shown). In this study, in some cases, the MeOHextract and its EtOAc subfraction exhibited higher antibacterial activity com-pared with streptomycin, while tetracycline showed higher activity in someother cases than the solvent fractions. No inhibitory effect was observedagainst three gram-negative bacteria: E. coli 0157:H7 ATCC 43888, S. enter-itidis KCTC 12021 and S. typhimurium KCTC 2515. As shown in Table 2, theMIC values of the MeOH extract against the tested bacteria were found in the125–500 mg/mL range. The MIC values for EtOAc fraction were found moresusceptible to S. aureus KCTC 1916 and ATCC 6538, and L. monocytogenesATCC 19116, ATCC 19118 and ATCC 19166 (62.5–125 mg/mL) than those ofB. subtilis ATCC 6633, P. aeruginosa KCTC 2004 and E. coli ATCC 8739


(250 mg/mL for each). Strong inhibition of BuOH fraction against L. mono-cytogenes ATCC 19116, S. aureus KCTC 1916 and ATCC 6538 was alsoobserved (MIC values of 125 mg/mL), as shown in Table 2. The highestantibacterial activity was detected in the EtOAc fraction by MICs as comparedwith other fractions. L. monocytogenes (ATCC 19116 and ATCC 19118) andS. aureus (KCTC 1916 and ATCC 6538) were found to be the most sensitiveamong the organisms tested.

A previous report showed that the fruit extract of A. altissima Swingleoccurring in China inhibited weakly the growth of E. coli, S. aureus, P.

TABLE 1.ANTIBACTERIAL ACTIVITY OF AILANTHUS ALTISSIMA SWINGLE LEAVE EXTRACTS

AGAINST FOODBORNE PATHOGENS AND SPOILING BACTERIA

Microorganism MeOHextract*

Subfractions of MeOH extract* Antibiotic†

CHCl3 EtOAc BuOH S T

ListeriamonocytogenesATCC 19116

18.2 � 0.7 14.1 � 0.7 17.2 � 0.7 14.4 � 0.5 14.2 � 0.9 20.2 � 1.5

L. monocytogenesATCC 19118

15.2 � 0.5 14.3 � 0.5 16.1 � 1.4 14.2 � 1.5 14.5 � 1.1 16.3 � 0.7

L. monocytogenesATCC 19166

14.2 � 0.5 12.1 � 0.7 14.2 � 0.7 13.4 � 0.5 14.1 � 0.6 19.0 � 0.5

Staphylococcusaureus KCTC1916

16.2 � 0.7 13.2 � 1.1 23.2 � 1.2 15.0 � 1.4 16.1 � 0.9 18.1 � 0.5

S. aureus ATCC6538

14.1 � 0.5 13.1 � 1.1 14.0 � 2.1 14.2 � 0.9 14.2 � 0.6 19.2 � 0.6

Bacillus subtilisATCC 6633

13.2 � 0.5 nd 14.1 � 0.7 13.3 � 1.4 15.3 � 0.2 18.1 � 0.5

PseudomonasaeruginosaKCTC 2004

12.1 � 1.1 12.3 � 0.5 14.2 � 2.1 13.2 � 0.7 19.2 � 0.4 20.3 � 1.0

Escherichia coliATCC 8739

12.2 � 0.7 nd 12.2 � 1.2 12.1 � 1.4 24.2 � 0.9 17.3 � 1.5

E. coli 0157:H7ATCC 43888

nd nd nd nd 15.3 � 0.9 20.1 � 0.5

SalmonellaenteritidisKCTC 12021

nd nd nd nd 14.3 � 0.6 21.4 � 1.0

SalmonellatyphimuriumKCTC 2515

nd nd nd nd 13.2 � 0.2 21.2 � 0.6

Values are represented as mean � SD of triplicate experiments.* Diameter of inhibition zone, including diameter of disk 6 mm (tested at a volume of 0.5 mg/disk).† S, streptomycin (10 mg/disk); T, tetracycline (10 mg/disk).nd, no detection; MeOH, methanol; CHCl3, chloroform; EtOAc, ethyl acetate; BuOH, butanol.


aeruginosa and S. typhimuriun, with inhibition zones of 6.87–7.51 mm,using the concentration of ethanol extract of 1.2 mg/mL (Zhao et al. 2005).Our leaf extracts of A. altissima Swingle occurring in Korea demonstratedsignificantly higher antibacterial activity against some foodborne pathogenssuch as L. monocytogenes, S. aureus, B. subtilis, P. aeruginosa and E. coli(inhibition zones 12.1–23.2 mm) at the concentration of extracts 0.5 mg/disk. It is recognized that chemical composition of the plant or herbal prod-ucts may be very changeable because of variations in origin, species, growth,harvesting and processing conditions, thereby altering the biological activi-ties studied (Vardar-Unlu et al. 2003). Experimental results indicated that theextracts showed inhibitory activity against all six gram-positive and twogram-negative bacteria tested. Therefore, gram-positive bacteria were foundto be more sensitive toward plant extracts. When comparing the dataobtained from different studies, most publications provide a generalizationon whether or not a plant extract possesses activity against gram-positive andgram-negative bacteria. However, few provide details on the extent or spec-trum of this activity. Karaman et al. (2003) observed that gram-positive bac-teria were more sensitive to plant extracts than gram-negative bacteria. Theirhigher resistance among gram-negative bacteria has been ascribed to thepresence of their outer phospholipidic membrane, almost impermeable tolipophilic compounds (Nikaido and Vaara 1985). This is the reason whygram-positive bacteria were found to be more sensitive to the MeOH extract

TABLE 2.MIC* VALUES OF AILANTHUS ALTISSIMA SWINGLE LEAVE EXTRACTS AGAINST

FOODBORNE PATHOGENS AND SPOILING BACTERIA

Microorganism MeOH extract Subfractions of MeOH extract

CHCl3 EtOAc BuOH

Listeria monocytogenes ATCC 19116 125 250 125 125L. monocytogenes ATCC 19118 125 250 125 250L. monocytogenes ATCC 19166 500 500 125 250Staphylococcus aureus KCTC 1916 125 250 62.5 125S. aureus ATCC 6538 250 250 125 125Bacillus subtilis ATCC 6633 500 nd 250 500Pseudomonas aeruginosa KCTC 2004 250 500 250 250Escherichia coli ATCC 8739 500 nd 250 500E. coli O157:H7 ATCC 43888 nd nd nd ndSalmonella enteritidis KCTC 12021 nd nd nd ndSalmonella typhimurium KCTC 2515 nd nd nd nd

* Values in mg/mL.nd, no detection; MIC, minimum inhibitory concentration; MeOH, methanol; CHCl3, chloroform;EtOAc, ethyl acetate; BuOH, butanol.


and various MeOH-derived subfractions of A. altissima Swingle thangram-negative bacteria.

Foodborne diseases caused by gram-positive bacteria such as S. aureus,L. monocytogenes and B. subtilis are most commonly reported (McCabe-Sellers and Samuel 2004). L. monocytogenes is responsible for severe food-borne illness, such as listeriosis. Most reports associate listeriosis with theconsumption of contaminated ready-to-eat foods such as dairy products, pro-cessed or cured meat and poultry, seafood and uncooked eggs (Garcia et al.2004). Our groups are interested in screening plant materials to identify naturalantimicrobial agents to reduce foodborne pathogens so they could therefore beused in food industries as natural preservatives or flavoring agents. As part ofthese studies, we previously investigated antilisterial properties of garlic shootjuice (Kim et al. 2007). In recent years, many researchers screened the anti-microbial activity of plant extracts using various concentrations of the extracts.Al-Fatimi et al. (2007) reported the antimicrobial activity of 27 medicinalplants and found inhibition zones of 8–25 mm at the concentrations of extractsof 2 mg/disk. Duraipandiyan and Ignacimuthu (2007) found the inhibitionzones of 8–23 mm against some bacteria using the concentrations of a medici-nal plant (Cassia fistula) extract of 1.25, 2.5 and 5 mg/disk. In this study, weinvestigated the antibacterial activity of medicinal plant (A. altissima Swingle)extracts using a comparatively low concentration of the extract (0.5 mg/disk),and we observed a diameter of inhibition zones of 12.1–23.2 mm against somefoodborne pathogens and spoiling bacteria.

Free radical scavenging activity of MeOH extract and its subfractions,measured by the DPPH assay is shown Table 3. The activity of the plant

TABLE 3.FREE RADICAL SCAVENGING ACTIVITY (DPPH) AND

TOTAL PHENOLIC COMPOUNDS (mg/g DRY WEIGHT) OFLEAVES OF AILANTHUS ALTISSIMA SWINGLE

Sample IC50 (mg/mL) Total phenolic(mg GAE/g dw)

Methanol extract 35.46 � 2.1 71.63 � 2.2Hexane fraction 168.16 � 3.2 24.87 � 1.8Chloroform fraction 53.18 � 1.5 39.43 � 0.8Ethyl acetate fraction 16.45 � 2.9 122.53 � 2.6Butanol fraction 28.70 � 0.6 85.10 � 1.9Ascorbic acid (control) 6.55 � 0.9 naBHA(control) 18.27 � 1.3 na

Values are given as mean � standard deviation of triplicateexperiments.BHA, butylated hydroxyanisole; na, not applicable; GAE, gallicacid equivalents; DPPH, 1,1-diphenyl-2-picrylhydrazyl.


extracts is concentration-dependent, and the lower IC50 value reflects betterprotective action. The IC50 values of MeOH extract and its various organicsubfractions were recorded in the 16.45–168.16 mg/mL range. Polar subfrac-tions of MeOH extract (e.g., EtOAc and BuOH fraction) exhibited strongerDPPH scavenging activity than nonpolar fraction. The free radical scavengingactivity of EtOAc acetate fraction (IC50 = 16.45 mg/mL) was superior to allother fractions. The IC50 value of EtOAc fraction (IC50 = 16.45 mg/mL) waslower than synthetic antioxidant BHA (IC50 = 18.27 mg/mL). The strongestactivity of the EtOAc fraction may be related to its higher phenolic content(122.53 mg GAE/g) as measured by the gallic acid test (Table 3).

The total phenolic content of MeOH extract and its fractions were foundin the range of 24.87–122.53 mg GAE/g of dry sample (Table 3). The totalphenolic content of MeOH extract was 71.63 mg GAE/g and its subfractionsincluding hexane, CHCl3, EtOAc and BuOH were 2.48, 3.94, 12.25 and 8.51%of dry sample, respectively. These results showed that the total phenoliccontent in EtOAc fraction (12.25%) was the highest compared with otherextracts. This may be due to the presence of high bioactive compounds inEtOAc fraction. The previously mentioned high total phenolic constituent ofthe EtOAc fraction also supports the strongest radical scavenging activity ofthe EtOAc fraction, suggesting that activity is mostly related to its water-soluble phenolic compounds.

Our results showed interesting antibacterial and antioxidant activity ofthe methanolic extract and its various fractions from A. altissima Swingle. Thisis probably due to polyphenol substances present in the extract. The antimi-crobial activity of phenolic compounds is well documented (Karamanoli2002). Polyphenols are the major compounds with antioxidant activity,although they are not the only ones. Thus, active phenolic compounds mighthave several invasive targets that could lead to their inhibition of bacteria.

Antioxidative and antimicrobial properties of the plant extracts are ofgreat interest in both the academia and the food industry because their pos-sible uses as natural additives emerged from a growing tendency to replacesynthetic chemicals by natural ones. The results demonstrated that theextracts from A. altissima Swingle exerted significant antibacterial and anti-oxidant properties. Owing to its strong inhibitory activity against foodbornepathogens and excellent protective features exhibited in antioxidant activitytests, the extracts from the A. altissima Swingle could be concluded as anatural source that can be used as food antimicrobial preservatives. Our find-ings introduce a unique natural source that possesses strong antibacterial andantioxidant substances with potential applications in the food industry.Further studies are required to assess the efficacy of extracts in foods andtheir toxicity to humans because medicinal plants do not have GenerallyRegarded as Safe status.


ACKNOWLEDGMENT

This work was supported by a grant from the Regional Innovation CenterProgram of MOCIE, Korea.

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