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Han Ching Voon, Rajeev Bhat, and Gulam Rusul Abstract: Plants with potential therapeutic value have been used from time immemorial to cure various ailments and infectious diseases. Secondary metabolites or the bioactive compounds (phytochemicals) present in plants have been reported to be accountable for various observed biological activities. Consumer awareness of the possible side effects of using chemical-based antimicrobial agents has forced researchers to identify and explore natural plant-based antimicrobial agents (or preservatives) that are toxicologically safe, especially when used in food applications. Of late, scientic evidence has been provided on the potential antimicrobial activities exhibited by certain traditionally used ower extracts or their essential oils (edible and wild). This review focuses on providing and updating available information on the antimicrobial activities exhibited by owers, which are envisaged to nd potential applications as natural preservatives for foods or applications in the pharmaceutical industries to develop new and economical herbal-based products for treating various diseases.
Introduction
Infectious diseases and foodborne illnesses can cause severe health effects and can even lead to death among the residing population, especially in the developing regions of the world. The continual emergence of antibiotic-resistant microorganisms has prompted researchers world over to search for new antimicrobial agents that are more effective against the resistant microbial pathogens (Nascimento and others 2000; Thaller and others 2010). Structural modication of the antimicrobials (against which microbial resistance has been developed) is reported to improve the effectiveness of antimicrobial agents against bacteria, fungi, and viruses (De Clercq 2001; Poole 2001; Jeu and others 2003; Zhang and others 2010). However, of late, research efforts have been put forth to improve the effectiveness of antimicrobial drugs by developing novel and a new class of antimicrobial drugs that can effectively work on multitargeted sites or organisms (Esterhuizen and others 2006; Alka and others 2010). Traditionally, plants with potential therapeutic or medicinal values have been successfully utilized for preventing and treating various ailments and foodborne illnesses. Since time immemorial, various plants and their products have been used in traditional medicine to cure some of the common disorders and degenerative diseases in humans as well as in animals (such as Ayurvedic and traditional Chinese medicinal practices). The effectiveness of these
procedures has been attributed mainly to the presence of active phytochemicals or bioactive compounds in plants (Quarenghi and others 2000; Ye and others 2004; Zhang and Zhang 2007; Dung and others 2008; Zhao and others 2009). Given the scope of searching new antimicrobial agents, antimicrobials derived from plant materials are often regarded as natural and safe compared to industrial chemicals. Of late, plant-based medicine has become more popular due to the increasing concern of consumers with regard to the use of synthetic chemical preparations and use of articial antimicrobial preservatives, especially in modern food protection practices (Marino and others 2001; Hamedo and Abdelmigid 2009). Some of the hoped-for advantages of using natural antimicrobials include: reducing total dependence on antibiotics, reducing development of antibiotic resistance by pathogenic microorganisms, controlling cross-contaminations by foodborne pathogens, improvizing food preservation technology, and strengthening immune system in humans (Abou-taleb and Kawai 2008; Fisher and Phillips 2008; Tajkarimi and others 2010). Today, growing market trends indicate a rapid increase in the number of natural plant-derived products (such as green tea, herbal decoctions, or herbal medicines) that may include aerial parts, seeds, fruits, roots, rhizomes, and owers. Among these, owers have attained high priority and found various applications. Floral extracts and their isolated essential oils are traditionally believed to be rich in phytochemicals exhibiting rich bioactivity. These compounds are MS 20110898 Submitted 7/26/2011, Accepted 9/26/2011. Authors are of interest to the local industry as well as to the general popwith Food Technology Div., School of Industrial Technology, Univ. Sains Malaysia, Penang 11800, Malaysia. Direct inquiries to author Bhat (E-mail: ulation and are actively being explored for various commercial applications (such as tea, bakery products, and more). Floral exrajeevbhat1304@gmail.com and rajeevbhat@usm.my). tracts and essential oils are also considered to be potential natural
34 Comprehensive Reviews in Food Science and Food Safety r Vol. 11, 2012
c 2011 Institute of Food Technologists doi: 10.1111/j.1541-4337.2011.00169.x
Extraction Method
Solvent extraction Solvent extraction is one of the most widely employed methods for preparation of ower extracts. Solvent extraction (solid-liquid extraction) involves the process of leaching (simple physical solution or dissolution process). Leaching is a separation technique that involves removal of soluble solids from a solid mixture by employing a suitable solvent or solvent mixture. Various factors inuence the solvent extraction procedure, which includes: the rate of transport of solvent into the material, rate of solubilization of soluble constituents in the solvent, and the rate of transport of solution (extract) out of the insoluble matter. Solvent polarity, vapor pressure, and viscosity are also of importance for effective extraction. In case of plant materials, adequate time is required for diffusion of solvent via plant cell walls for dissolution of soluble constituents and for diffusion of the solution (extract) out to the surface of the cell wall (Houghton and Raman 1998; Singh 2008; Wijekoon and others 2011). Flower extracts can be prepared either from fresh or dried samples. Prior to extraction, ower samples are subjected to air-drying or freeze-drying, followed by grinding, milling, or homogenization to reduce sample particle size. These procedures are followed in order to enhance the efciency of extraction process and yield of the resulting extract. Various solvents, such as methanol, ethanol, hexane, acetone, ethyl acetate, chloroform are commonly used for extraction (either in the pure form or after dilution with distilled water) (Dai and Mumper 2010). Choice of selecting a solvent mainly depends on the solubility of the bioactive constituents, safety aspects, and potentials involved for artifact formations (Jones and Kinghorn 2005). Maintaining the stability of bioactive compounds is vital while selecting an appropriate and efcient extraction method as some of the compounds (mainly those of phenolics) tends to get oxidized and degraded at high temperature or on prolonging the extraction time (Robards 2003; Dai and Mumper 2010). Besides, an optimized value of sample-tosolvent ratio needs to be standardized, which involves equilibrium between avoidance of saturation effects, solvent wastes, and costs incurred (Pinelo and others 2006; Dai and Mumper 2010). Magnetic stirring and continuous rotary shaking are also employed in certain cases to enhance molecular interactions during extraction process. Usually, to ensure maximum extraction of bioactive compounds, the extraction process is repeated 2 or 3 times and the extracts are pooled together (Guill en and others 1996; Stalikas 2007). Followed by this, the extracts are ltered and centrifuged to remove any oating particulate matters. In order to prevent formation of artifacts and degradation or polymerization of phenolic compounds, ower extract should not be stored in the solvent at room temperature or exposed to direct sunlight for a long time duration. Once done, extracts are freeze dried or concentrated
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Methods for determining antimicrobial activity of oral extracts and essential oils Various conventional methods are routinely employed for determining the antimicrobial activity of oral extracts and essential oils. Generally, in vitro assays are employed. The agar diffusion method (paper disc or well) and dilution method (agar or broth) are the 2 most common techniques used. Agar diffusion method. The agar diffusion method is one of the most widely employed techniques for evaluating antimicrobial activity. In this technique, agar plates are inoculated with test microorganisms (usually pathogenic microbes). Floral extracts or essential oils are applied directly onto paper discs, which are then placed on the agar medium or into wells made in the agar. The agar plates are incubated to allow the components of oral extracts or essential oils to diffuse into the agar medium. The diameter of growth inhibition zones around the discs or wells is then considered to be an indication of the effectiveness of the material being tested (Kalemba and Kunicka 2003; Holley and Patel 2005). Dilution method. In this method, agar broth cultures (in Petri dishes or test tubes) and liquid broth cultures (in conical asks or test tubes or by microtiter plate-broth microdilution method) are used for determining antimicrobial activities. The inhibitory effect of the extracts or essential oils are measured based on turbidimetry or the plate count method. The obtained result is expressed as growth inhibition index (percentage growth inhibition compared to the control cultures without extract or essential oil) or minimum inhibitory concentration, MIC (lowest concentrations of extract or essential oil that can inhibit the growth of microorganisms). In some of the reports (Dung and others 2008; Abdoul-Latif and others 2010) minimum lethality concentration (MLC, the lowest concentration of extract or essential oil that kills or totally inhibits a microorganism), minimum bactericidal concentration (MBC) or minimum fungicidal concentration (MFC) is computed. The microorganisms from agar broth or liquid broth where no growth occurs are observed and are transferred into a new medium and incubated for a certain xed period of time. In some instances, MLC is considered to be a concentration that leads to >99.9% reduction in the number of microorganisms originally inoculated (Kalemba and Kunicka 2003; Holley and Patel 2005).
Allium species Allium spp. belongs to the largest genus (Allium, Alliaceae family) that is comprised of nearly 450 species and is found distributed widely in the northern hemisphere (Lonzotti 2006). However, most of the plants belonging to the Allium genus are consumed regularly in many Asia-Pacic regions. The plants and their parts are used in cooking because of their characteristic avor, attributed due to sulfur-based compounds (Tada and others 1988). Evaluation of antimicrobial activity has been reported to support the therapeutic value of these species as anti-infective agents (Chehregani and others 2007). The effective antimicrobial activities (of the aqueous extracts) of different parts of Allium spp. (bulbs, leaves, owers, rhizomes) against pathogenic bacteria such as Shigella exinix, Klebsiella pneumoniae, Bacillus subtilis, Bacillus cereus, Staphylococcus aureus, and Escherichia coli have been reported based on agar disc diffusion and serial dilution methods (Chehregani and others 2007). The reported diameter of inhibition zones for Allium atroviolaceum, Allium eriophyllum, Allium scabriscapum, Allium stamineum, Allium iranicum, and Allium shelkovnikovii ranged from 8.5 to 36.2 mm, 6.4 to 36.8 mm, 5.4 to 25.3 mm, 4.4 to 39.7 mm, 3.9 to 28.3 mm, and 0.0 to 27.8 mm. Moreover, the ower extracts of some Allium spp. (A. scabriscapum, A. iranicum, A. shelkovnokovii) exhibited much higher antibacterial activity than the bulb extracts with MIC values (ranging from 0.625 to 5.00 mg/mL, 2.50 to 12.50 mg/mL, and 2.5 to 10.00 mg/mL), indicating that the tannin accumulated in the owers to have played a role in exhibiting the antimicrobial activities. While the bulbs of Allium spp. are known for their high antibacterial activities, the results of this study indicated that the oral extracts from Allium spp. also have high potential for use as antibacterial agents. Alpinia galanga (Linn.) Swartz. (greater galangal) Alpinia galangal (family: Zingiberaceae) is a stemless perennial herb indigenous to South-East Asia and Indonesia. The plant bears large white owers with a pleasant fragrance (Yang and Eilerman 1999). Galangal plant parts have been traditionally used in China and Thailand to relieve gastrointestinal pain and to treat maladies involving fungi (Yang and Eilerman 1999; Oonmetta-aree and others 2006). The owers are either consumed raw or made into pickles in Asian cuisine (Yang and Eilerman 1999; Raina and others 2002; Tonwitowat 2008). The plants rhizome is extensively used in Thai cooking for its unique ginger-like avor accompanied with a tinge of pungent and peppery odor (Juntachote and others 2007). Furthermore, this plants rhizome is also used for medicinal purposes, which is reported to exhibit antifungal, antigardial, antiamebic, antimicrobial, and antioxidant activities (Juntachote and Berghofer 2005;Phongpaichit and others 2005; Oonmetta-aree and others 2006; Voravuthikunchai and others 2006; Juntachote and others 2007; Hsu and others 2010).
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Table 1Some selected reports on antimicrobial activities of edible owers. Solvent used Water Hexane and ethanol Methanol Methanol, chloroform, hexane, and distilled water Hexane, chloroform, ethyl acetate, methanol, and water 4-hydroxy benzoic acid hydrate Antibacterial and antifungal activity Antibacterial and antifungal activity Antibacterial activity Antibacterial activity Antibacterial activity Major antimicrobial component Activity Sensitive microorganism Reference
Plant
2011 Institute of Food Technologists S. exinix, K. pneumoniae, B. Chehregani and subtilis, B. cereus, S. aureus, E. coli others (2007) L. monocytogenes, S. aureus, S. Hsu and others sonnei, S. boydii, S. dysenteriae (2010) Quarenghi and others (2000) Mann and others (2011) Methanol Antibacterial and antifungal activity Sangetha and others (2008) Hexane, chloroform, ethyl acetate, methanol, and water rhein (1, 8-dihydroxyanthraquinone-3carboxylic acid) Antifungal activity Hydro-alcohol and chloroform Methanol Antibacterial and antifungal activity Antibacterial and antifungal activity Bhalodia and others (2011) Sangetha and others (2008) Antibacterial and antifungal activity Antibacterial and antifungal activity Antibacterial activity S. aureus, S. epidermidis, M. luteus, E. coli, P. aeruginosa, P. vulgaris Methanol and hexane: S. aureus, E. coli, A. niger Chloroform: E. coli, A. niger Distilled water: S. aureus, E. coli Hexane, chloroform, ethyl acetate, methanol, water: S. aureus, S. epidermidis, B. subtilis, E. faecalis, P. aeruginosa 4- hydroxyl benzoic acid hydrate: T. mentagrophytes, and E. occosum P. mirabilis, S. aureus, B. thuringiensis, S. typhi, Micrococcus spp., E. aerogenes, B. subtilis, S. sonnei, A. lipoferum, K. pneumoniae, P. aeruginosa, C. albicans, A. niger Hexane, chloro-form, methanol, water: Not tested Ethyl acetate: T. mentagrophytes, T. simii, T. rubrum, E. occosum, Scopulariopsis spp. Rhein: T. mentagrophytes, T. simii, T. rubrum, E. occosum, Scopulariopsis spp. S. aureus, S. pyogenes, E. coli, P. aeruginosa, A. niger, A. clavatus, C. albicans P. mirabilis, S. aureus, E. coli, S. typhi, Micrococcus spp., E. aerogenes, B. subtilis, S. sonnei, A. lipoferum, K. pneumoniae, P. aeruginosa, C. albicans, A. niger P. aeruginosa, E. coli, B. subtilis, S. aureus,K. pneumoniae, S. epidermidis, P. vulgaris, S. paratyphi-A serotype, C. albicans P. aeruginosa, E. faecalis, S. exneri, S. epidermidis, S. saprophiticus, E. cloaceae, S. marcescens C. parapsilosis, C neoformans S. epidermidis and B. subtilis Sassi and others (2008a) Sassi and others (2008b)
Anthemis cotula (Stinking chamomile) Bombax buonopozense P Beauv. (Gold Coast bombax)
Blending at room temperature Shaking on an orbital shaker at room temperature for 24 h Solvent extraction
Soxhlet extraction
Maceration for 48 h (3) Petroleum ether, ethyl for organic extraction; acetate, methanol, and hot boiling for 1 h for water water extraction Hydrodistillation with a Clevenger apparatus for 5 h
Vol. 11, 2012 r Comprehensive Reviews in Food Science and Food Safety 37
continued
Table 1Continued. Solvent used 80% methanol Petroleum ether, ethyl acetate, and methanol Antibacterial activity Antibacterial activity Antibacterial activity B. cereus, L. monocytogenes, E. coli, S. anatum Major antimicrobial component Activity Sensitive microorganism Reference Shan and others (2007) Zhao and others (2009) Dung and others (2008)
Plant
Shaking in water bath at room temperature for 24 h Soxhlet extraction for 1 h (3)
Essential oil isolation: Ethanol hydrodistillation with a modied Clevenger apparatus for 4 h. Solvent extraction: ethanol extraction (3) at room temperature
Cnicus benedictus Linn. (Blessed thistle) Water and methanol Ethyl acetate, ethanol, and petroleum ether
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Petroleum ether: S. aureus, MRSA Ethyl acetate: S. aureus Methanol: Nil Essential oil: B. subtilis, P. aeruginosa (FS); S. aureus, L. monocytogenes, E. aerogenes, S. Typhimurium, S. enteritidis, E.coli, E. coli O157:H7 (FB); S. aureus, S. epidermidis, E. coli, C. albicans (SP); MRSA; E. faecium (VRE); A. baumannii, E. coli, E. cloacae, K. pneumoniae, P. aeruginosa, S. marcescens, S. aureus (MARB) Ethanol: B. subtilis, P. aeruginosa (FS); S. aureus, L. monocytogenes, (FB); S. aureus, S. epidermidis (SP); MRSA; E. faecium (VRE); A. baumannii, S. aureus (MARB) S. Typhimurium, S. enteritidis, S. aureus, E. coli, S. pyogenes, P. aeruginosa, B. proteus, S. sonnei H. pylori Nakhaei and others (2008) Vahidi and others (2002) Antibacterial activity Antibacterial activity Antibacterial and antifungal activity Antibacterial activity Antibacterial activity Antifungal activity Antibacterial activity Ethanol, chloroform, and distilled water 80% methanol Chouhan and Singh (2010) Uma Devi and others (2009) Lachumy and others (2010) Stonsauvapak and others (2000) B. cereus, L. monocytogenes, S. aureus, E. coli, S. anatum A. niger, A. fumigatus S. Typhimurium, S. aureus, Enterococcus spp., E. coli Shan and others (2007) Bansod and Rai (2008) Ushimaru and others (2007)
continued
Maceration for 3 d
Maceration for 48 h
Crotalaria juncea L. (Sunn hemp) Dendrobium nobile (Dendrobium) Etlingera elatior (Torch ginger)
Eugenia caryophyllata Thunb. or Syzygium aromaticum (Clove) 80% methanol 70% methanol
Ethyl acetate: S. aureus, S. epidermidis, E. coli, M. luteus, C. albicans, Cladosporium spp., and A. niger Ethanol: Nil Petroleum ether: Cladosporium spp. E. coli, K. pneumoniae, P. aeruginosa, S. aureus, V. cholare E. coli, B. subtilis, Proteus, S. typhi, and S. aureus S. aureus, B. thuringiensis, E. coli, Salmonella spp., P. mirabilis, Micrococcus spp., B. subtilis, C. albicans, A. niger. E. coli O157: H7, Y. enterocolitica
Shaking in water bath at room temperature for 24 h Hydrodistillation with a Clevenger apparatus for 5 h Solvent extraction
Table 1Continued. Solvent used Methanol Antibacterial and antifungal activity Antibacterial activity Major antimicrobial component Activity Sensitive microorganism Reference
Plant
2011 Institute of Food Technologists S. aureus, Micrococcus spp., B. Rajeh and others subtilis, B. thuringiensis, E. coli, K. (2010) pneumoniae, S. typhi, P. mirabilis B. cereus, E. faecalis, S. epidermidis, Drewes and Van S. aureus, methicillin- and Vuuren (2008) gentamycin-resistant S. aureus, E. coli, K. pneumoniae, P. aeruginosa, C. neoformans, C. albicans Distilled water and ethanol Methanol 2-hydroxy-4,6dibenzyloxychalcone,5,7dibenzyloxyavanone, 1-[2,4,6-trihydroxy-3-(2hydroxy-3-methyl-3-butenyl)phenyl]-1-propanone, acylphloroglucinol derivative, 3-methoxyquercetin and 4-O-glucose derivative of 2-hydroxy-6-methoxy chalcone Antibacterial activity Antibacterial activity B. cereus S. sanguinis 80% methanol Methanol Antibacterial activity Antibacterial activity B. cereus, S. aureus, S. anatum S. sanguinis Shan and others (2007) Tsai and others (2008) Antibacterial activity Rahman and Kang (2009) Antibacterial activity Antibacterial activity Rhee and others (2011) L. monocytogenes, B. subtilis, B. cereus, S. aureus, S. enteritidis, S. Typhimurium, E. aerogenes and E. coli B. fragilis, B. ovatus, C. difcile, C. perfringenes, P. acnes, Peptostreptococci S. aureus, E. coli, P. aeruginosa, K. pneumoniae
Maceration for 14 d
Soaking for 20 min and blending for 3 min Solvent extraction for 3 h (and re- extraction overnight) at room temperature Shaking in water bath at room temperature for 24 h Solvent extraction for 3 h (and re- extraction overnight) at room temperature Hydrodistillation with a Clevenger apparatus for 3 h
Reux with distilled water n- butanol and partitioning with n-butanol Essential oil isolation: Ethanol hydrodistillation with a Clevenger apparatus for 4 h. Solvent extraction: maceration
Vol. 11, 2012 r Comprehensive Reviews in Food Science and Food Safety 39
continued
Table 1Continued. Solvent used Major antimicrobial component Activity Sensitive microorganism Reference Talreja (2010) Hassan and others (2009)
Plant
Soxhlet extraction for 24 h 80% ethanol Hot water and 80% ethanol
Moringa oleifera (Horseradish tree) Nymphaea lotus Linn. (Egyptian white water-lily)
Plumeria alba Linn. (White champa) Petroleum ether, alcohol, and water Antibacterial activity Antibacterial activity
B. subtilis, S. aureus, E. coli, K. pneumoniae, and C. albicans MRSA, multi-drug-resistant P. aeruginosa, enterohemorrhagic E. coli O157 EHEC, S. typhi, P. vulgaris, K. pneumoniae, B. subtilis, C. albicans, A. niger S. aureus, B. subtilis, P. aeruginosa, S. typhi
40 Comprehensive Reviews in Food Science and Food Safety r Vol. 11, 2012
Antibacterial activity Antibacterial activity Antibacterial and antifungal activity Antibacterial activity Hexane, chloroform, and methanol Petroleum ether, ether, chloroform, methanol, and ethanol Ethanol S. aureus, E. coli, P. aeruginosa, K. pneumoniae Pirbalouti and others (2010) Methanol Antibacterial and antifungal activity Antibacterial activity Ksouri and others (2009) Pirbalouti and others (2010) Ethanol S. epidermidis, S. aureus, M. luteus, E. coli, P. aeruginosa, C. kefyr, C. holmii, C. albicans, C. sake, C. glabrata S. aureus, E. coli, P. aeruginosa, K. pneumoniae Methanol and ethyl acetate Antibacterial and antifungal activity B. cereus, B. subtilis, S. aureus, S. Abe and others epidermidis, S. faecalis, C. (2004) albicans, C. tropicalis, C. glabata, Z. rouxii, S. cerevisiae, A. fumigatus, P. frequentans
E. coli, S. pneumoniae, S. Hirulkar and Agrawal Typhimurium, E. aerogenes, P. (2010) vulgaris, S. aureus, S. epidermidis, B.subtilis, C. freundii, P. aeruginosa C. macginleyi Koday and others (2010) K. pneumoniae, S. pneumoniae, S. Mostafa and others pyogenes, S. aureus, E. coli, P. (2011) aeruginosa S. aureus, S. lutea, B. cereus, E. coli, Ioannou and others C. albicans (2007)
Hydrodistillation with a modied Clevenger apparatus for 3 h Essential oil isolation: hydrodistillation with a Clevenger apparatus for 4 h. Solvent extraction: maceration Magnetic stirring for 30 min
Essential oil isolation: hydrodistillation with a Clevenger apparatus for 4 h. Solvent extraction: maceration Blending
Therapeutic values Edible flowers (used in treatment of gastrointestinal pain, dysentery, gout, fever, muscle aches, skin diseases, liver disorder, etc.)
Pharmaceutical values (exhibit analgesic, anti-inflammatory, antioxidant, anticancer, antitumor, anti-hyperglycemic, astringent activities, etc.)
Antimicrobial activities
Spoilage microorganisms (A. niger, B. subtilis, C. kefyr, C. holmii, E. aerogenes, E. faecalis, H. alvei, P. aeruginosa, S. marcescens, S. cerevisiae, Z. rouxii, etc.)
Pathogenic microorganisms (C. albicans, E. coli O157:H7, L. monocytogenes, S. aureus, S. Typhimurium, S. enteritidis, S. epidermidis, T. mentagrophytes, T. simii, rubrum, Scopulariopsis spp., etc.) T.
- Preservatives - Development of antimicrobial packaging (biopolymer based edible films) for food applications
- Antimicrobial agents
Figure 1Schematic representation of edible owers, their antimicrobial activities, and applications as natural antimicrobial agents.
By employing the agar disc diffusion method, antimicrobial activity of galangal ower buds against both Gram-positive and Gram-negative bacteria have been tested. The effects of drying methods (oven drying and freeze-drying) and solvents (hexane and ethanol) on the antimicrobial activity have also been investigated (Hsu and others 2010). Galangal was shown to be effective against Gram-positive bacteria (Listeria monocytogenes and S. aureus)
but exhibited little or no effect against Gram-negative bacteria (Salmonella spp., E. coli O157: H7, and Shigella spp.). Overall, antimicrobial activity of galangal was the highest for oven-dried samples extracted with ethanol (inhibition zone = 8.94 mm and MIC = 1.457 mg/mL) and the lowest for the freeze-dried samples extracted with ethanol (inhibition zone = 7.05 mm and MIC = 2.470 mg/mL). Due to its ability to inhibit the growth of
Vol. 11, 2012 r Comprehensive Reviews in Food Science and Food Safety 41
Figure 2Examples of some owers with known antimicrobial activities belonging to the species of: a = Clitoria ternatea; b = Cassia stula; c = Dendrobium nobile; d = Hibiscus spp.; e = Nelumbo spp.; f = Chrysanthemum spp.
Gram-positive bacteria, galangal ower buds have potential to be used as food, as building materials, for extracting dye, and also as a used as natural antimicrobial agent for preservation of perishable source of clothing ber. The decoctions prepared from leaves and roots are traditionally used to treat fever, muscle aches, pains, and foodstuffs. stomach discomforts (Akuodor and others 2011). Anthemis cotula L. (Stinking chamomile) Mann and others (2011) have evaluated antimicrobial activities Anthemis cotula (family: Asteraceae), a native of Europe and a of Bombax owers against S. aureus, E. coli, and A. niger using weed that grows extensively in Argentina, is commonly known the disc diffusion method. The results obtained clearly demonas Manzanilla del campo. Traditionally, A. cotula is believed strated antimicrobial activity of methanol, chloroform, hexane, to be effective for treatment of dysentery and gout. The de- and aqueous extracts against the 3 pathogens tested. However, the coctions made from the leaves and owers are reported to chloroform extract did not exhibit any activity against S. aureus exhibit insecticidal properties (Quarenghi and others 2000). and the aqueous extract showed no activity against A. niger. The The avonoid constituents present in this ower have been results of this study were able to provide scientic evidence to supreported to contain: quercetagetin, quercetagetin 7-glucoside, port the traditional uses of B. buonopozense for curing microbial quercetin, quercetin 7-glucoside, patuletin, patuletin 7-glucoside, infections. kaempferol, kaempferol 7-glucoside, and kaempferol 3-rutinoside (Quarenghi and others 2000). Cassia stula Linn. (golden shower tree) Quarenghi and others (2000) employed the agar disc diffuCassia stula (family: Leguminosae) is an ornamental tree found sion method to evaluate the antimicrobial activity of A. cotula in various parts of China, India, Mauritius, South Africa, Mexico, (methanol extract) against some of the pathogenic microbes, such the West Indies, East Africa, and Brazil. Various parts of this plant as S. aureus, Staphylococcus epidermidis, Micrococcus luteus, Streptococ- are used in the treatment of intestinal disorders, skin diseases, cus pneumoniae, E. coli, Pseudomonas aeruginosa, Proteus vulgaris, and such as leucoderma, liver problems, tuberculosis, hemetemesis, diSalmonella spp. Owing to the avonoid compounds present in the abetes, rheumatism, hypercholesterolemia, and diarrhea. The fruit ower, methanol extract at a concentration of 200 g/mL was pulp is used as a laxative, purgative, antipyretic, analgesic, and anfound to exhibit rich antimicrobial activities against the bacteria timicrobial agent in Indian Ayurvedic medicine. Its owers have tested (except for S. pneumoniae and Salmonella spp.) with diameters been reported to exhibit antifungal activities (to treat skin infecof inhibition zones ranging from 6.0 to 9.0 mm. tion) and are used to treat nasal infections in certain tribal sects (Perumal Samy and others 1998; Prashanth Kumar and others Bombax buonopozense P. Beauv. (Gold Coast Bombax) 2006; Duraipandiyan and Ignacimuthu 2007; Bhalodia and others Bombax buonopozense (family: Bombaceae) is a large tropical tree 2011). Also, owers have been reported to be useful in treating in Africa (found in Ghana, Uganda, and Gabon). The plant grows pruritus, burning sensation, dry cough, and bronchitis attributed up to 40-m high with large buttress roots, which are spread upto to its demulcent, lubricating, cooling, and emollient effects 6 m (Beentje and Sara 2001). This tree is also popular as Vabga (El-Saadany and others 1991; Duraipandiyan and Ignacimuthu in Ghana and Kurya in Northern Nigeria. The plant parts are 2007; Bhalodia and others 2011).
42 Comprehensive Reviews in Food Science and Food Safety r Vol. 11, 2012
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Cassia surattensis Burm.f. (Sunshine tree) Cassia surattensis (family: Leguminosae) is a owering plant native to South Asia, and found growing abundantly in India, Myanmar, Southern Pakistan, and Sri Lanka. The plants are grown as ornamental trees in tropical and subtropical regions. The bark and leaves of C. surattensis are believed to exhibit antiblenorrhagic properties (Sangetha and others 2008). In one of the experiments conducted by Sangetha and others (2008) on different parts (leaves, owers, stems, and pods) of C. stula and C. surattensis, all the bacteria and fungi studied (except Bacillus thuringiensis and S. cerevisiae) were susceptible to the methanol extract of C. surattensis owers with inhibition zones Chrysanthemum trifurcatum (Desf.) Batt. and Trab. ranging from 12 to 20 mm. Chrysanthemum trifurcatum (family: Asteraceae) is an herbal plant bearing small yellow owers. This plant is widely distributed in Chaerophyllum macropodum Boiss. (Chervil) Tunisia regions and the plant parts are used for treating constipaChaerophyllum macropodum (family: Apiaceae) is a biennial shrub tion, intestinal transit problems, and postdelivery pains (Sassi and with hard pinnate leaves. In Iran and Turkey, the edible vegetable others 2008b). The antimicrobial activity of petroleum ether, ethyl obtained from this plant is used as food and in the preparation acetate, methanol, and hot water extracts of Tunisian Chrysantheof cheese (Durmaz and others 2006; Coruh and others 2007; mum species against 5 Gram-positive and 9 Gram-negative bacEbrahimabadi and others 2010). The organic solvent extract from teria and 4 yeasts were evaluated by Sassi and others (2008a) the aerial parts of C. macropodum have been reported to exhibit by employing agar disc diffusion and microdilution assays. The
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Chrysanthemum morifolium Ramat. (Chrysanthemum) Chrysanthemum morifolium (family: Asteraceae) is an important medicinal herb of the Asteraceae family consisting of 8 major varieties (Hangju, Boju, Gongju, Chuju, Qiju, Huaiju, Jiju, and Hang ju). C. morifolium is traditionally used in China to protect the cardiovascular system, to lower blood glucose and fat levels, to regulate blood pressure, excrete lead, and to scavenge free radicals. This plant has been reported to exhibit signicant antibacterial, antioxidant, anti-inammatory, and anticancer activities. The bioactive compounds of C. morifolium consist of avonoids, sesquiterpenoids, chlorogenic acids, vitamins, and amino acids (Zhang and Zhang 2007; Zhao and others 2009). The methanolic extract of C. morifolium (inorescence) showed antimicrobial activity against B. cereus, L. monocytogenes, E. coli, and Salmonella anatum with inhibition zones in the range of 5.5 to 9.2 mm (Shan and others 2007). Besides, the antimicrobial activity of petroleum ether, ethyl acetate, and methanolic extracts of 7 species of C. morifolium owers cultivated in Kaifeng, China were tested against S. aureus and methicillin resistant S. aureus (MRSA) by the disc diffusion assay (Zhao and others 2009). Petroleum ether extracts of Mailang, Chunrijianshan, and Lengyan, as well as ethyl acetate extracts of Mailang, Chunrijianshan, Lengyan, Jianliuxiangbai, Guohuawansheng, and Changhong varieties showed good antibacterial activity on S. aureus with MIC of 125, 250, 250, 250, 250, 125, 250, and 250 g/disc, respectively. The petroleum ether extracts of Mailang, Chunrijianshan, and Lengyan were active against MRSA with MIC of 250 g/disc. All the extracts of Baiyudai did not exhibit any activity against S. aureus and MRSA at the tested concentration (250 g/disc). Also, the methanol extracts of all the species of C. morifolium did not show any antimicrobial activity. The authors have concluded that better antimicrobial activity was shown by yellow owers compared to purple and white owers.
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Cleistocalyx operculatus (Roxb.) Merr and Perry (water fairy ower) Cleistocalyx operculatus (family: Myrtaceae), also known as Eugenia operculata or Syzygium nervosum, is a perennial tree, widely distributed in China, Vietnam, and other tropical countries. Traditionally, the leaves and ower buds of the plant have been reported to be used as an ingredient in preparing certain beverages (tea decoctions) for treating gastrointestinal disorders and antisepsis (Dung and others 2008). In vivo and in vitro studies have shown the potentiality of C. operculatus buds to exhibit anticancer, antitumor, antihyperglycemic, and cardiotonic properties (Anthony and others 2002; Ye and others 2005; Mai and Chuyen 2007; Dung and others 2008). Results on the phytochemicals screening of ower buds have shown the presence of sterols, avanones, chalcones, triterpene acid, - sitosterol, and ursolic acids in the buds (Ye and others 2004; Dung and others 2008). Dung and others (2008), by using agar disc diffusion and microdilution susceptibility tests, have screened the effectiveness of the essential oil and ethanol extract of C. operculatus buds against 2 food spoilage bacteria (B. subtilis and P. aeruginosa), 9 foodborne pathogens (2 isolates of S. aureus, L. monocytogenes, Enterobacter aerogenes, Salmonella Typhimurium, Salmonella enteritidis, E. coli, and 2 isolates of E. coli O157:H7), 4 skin infectious pathogens (S. aureus, S. epidermidis, E. coli, and C. albicans), 3 methicillin-resistant S. aureus, 3 vancomycin-resistant Enterococcus faecium, and 15 multiantibiotic-resistant bacteria (2 isolates of Acinetobacter baumannii, 3 isolates of E. coli, 2 isolates of Enterobacter cloacae, 2 isolates of K. pneumoniae, 3 isolates of P. aeruginosa, 2 isolates of Serratia marcescens, and S. aureus). The essential oil of C. operculatus buds showed inhibition zones and MIC/MBC, which ranged from 8 to 16 mm and 1 to 20 L/ mL, respectively, effective against all the tested microorganisms. The ethanol extract demonstrated antimicrobial activity against all the Gram-positive bacteria and 1 food-spoilage Gram-negative bacterium (P. aeruginosa) with inhibition zones and MIC/MBC in the range of 8 to 22 mm and 0.25 to 32 mg/mL. Besides, in the cell viability assay of methicillin-
Clitoria ternatea Linn. (buttery pea, Asian pigeon wings) Clitoria ternatea (Family-Liguminoceae) is a tropical, perennial twining herb bearing blue or white colored owers (in single). This plant is extensively grown for ornamental and medicinal purpose in the Asian subcontinent (India, Bangladesh, Indonesia, Malaysia). In Malaysia, aqueous extract of the ower is used as a natural coloring agent for preparing dish from glutinous rice. The plant parts have been reported to exhibit anti-inammatory, antipyretic, antihyperlipidemic, analgesic, tranquilizing, and immunomodulatory activities (Mukherjee and others 2008; Solanki and Jain 2010, 2011, 2012). Root contains avonol glycosides, which exhibit rich antibacterial activity (Yadava and Verma2003). Cliotides (biologically active peptides) (present in owers, seeds, and nodules) have been isolated from heat-stable fractions of Clitoria ternatea extract. These cliotides showed potential antimicrobial activity against E. coli and cytotoxicity against HeLa cells (Nguyen and others 2011). Uma and others (2009) have screened the ower extracts (by maceration technique: solvents used methanol, chloroform, petroleum ether, hexane, and aqueous) of Clitorea ternatea against pathogenic microorganisms, such as uropathogenic, enteropathogenic, and enterotoxigenic E. coli, S. Typhimurium, S. enteritidis, K. pneumoniae, and Pseudomonas aureginosa. These microorganisms were isolated from patients with urinary tract infection and acute gastroenteritis. The method adopted for determining antimicrobial activity was disc diffusion method and minimum inhibitory concentration (two-fold serial dilution method). Results of this study revealed aqueous, methanol, and chloroform extracts to exhibit antimicrobial activity against uropathogenic, enteropathogenic, and enterotoxigenic E. coli, S. Typhimurium, K. pneumoniae, and P. aureginosa. However, no antibacterial activity was recorded for petroleum ether and hexane extracts. Cnicus benedictus Linn. (blessed thistle) Cnicus benedictus (family: Asteraceae) is the single species in the genus Cnicus; it is native to the Mediterranean region. This annual plant grows up to 60-cm high, and has leathery, hairy leaves (extending up to 30-cm long and 8-cm broad), with minute spines
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Crocus sativus Linn. (saffron) Crocus sativus (family: Iridaceae) has been used traditionally as a spice and as a food colorant in most of the countries over the world. Saffron, the worlds most expensive spice is obtained from the ower (mainly the stigmata) of the C. sativus plant. In folk medicine, saffron has been used as aphrodisiac, antispasmodic, and expectorant (Nakhaei and others 2008). Saffron is also used to treat atulence, colic, and abdominal pains, as well as to improve appetite and memory (Zhang and others 1994; Nakhaei and others 2008). Antitumor, radical scavenging, hyperlipemic, anticonvulsant, cytotoxic, antigenotoxic, and anti-ulcerogenic activities have been reported for C. sativus extracts or their chemical constituents (Nair and others 1995; Hosseinzadeh and Khosravan 2001; Abdullaev and others 2003; Al- moeh and others 2006; Nakhaei and others 2008). The biological properties of C. sativus are mainly attributed to crocin and saffranal, which are isolated from stigmata, leaves, petal, and pollen. Other isolated chemical constituents include crocetin, picrotoxin, quercetin, and kaempferol (Nakhaei and others 2008). According to Vahidi and others (2002), signicant antimicrobial activity was observed against S. epidermidis, C. albicans, Cladosporium spp., and A. niger when an ethyl acetate extract of stigmata of C. sativus was used. The inhibition zones and MIC ranged from 12 to 19 mm and 6.25 to 50 mg/mL, respectively. The ethyl acetate extract of stamens exhibited antimicrobial activity against S. aureus, S. epidermidis, E. coli, M. luteus, Cladosporium spp., and A. niger with inhibition zones and MIC ranging from 15 to 21 mm and 12.5 to 50 mg/mL, respectively.
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Crotalaria juncea Linn. (sunn hemp) Crotalaria juncea (family: Leguminoceae) plant parts (owers, buds, pods, and seeds) are commonly used as medicine and for culinary purposes (Bhatt and others 2009). The plant is widely distributed in tropical and subtropical regions, such as in India, Nepal, Sri Lanka, and Southern Africa. In Ayurvedic medicine, C. juncea has been used as an astringent, abortifacient, blood purier, demulcent, emetic, purgative, and for curing anemia, impetigo, menorrhagia, and psoriasis (Sharma and others 2001; Chouhan and Singh 2010). The seeds of C. juncea have been reported to exhibit signicant antispermatogenic, anti-ovulatory, and contraceptive activities (Vijaykumar and others 2004; Malashetty and Patil 2007). The chemical compounds isolated from the seeds of this plant were riddelline, seneciphylline, senecionine, trichodesmine, chodesmine alkaloids, galactose-specic lectin, and cardiogenin 3-O-[r]-d-xylopyranoside (Adams and Gianturco 1956; Chouhan and Singh 2010). Chouhan and Singh (2010) have reported antibacterial activity of the ethanolic extract of C. juncea owers against both Grampositive and Gram-negative bacteria by employing the agar disc diffusion assay. The extracts were found to be effective against E. coli, K. pneumoniae, P. aeruginosa, S. aureus, and Vibrio cholare (inhibition zone = 13, 14, 10, 13, and 8 mm). However, the extracts did not exhibit any activity against Citrobacter freundi, E. faecalis, Shigella exneri, and S. dysenteriae. Further, the authors have reported on the presence of steroids, triterpenes, avonoids, phenolics, and glycosides in the ethanol extract. Dendrobium nobile Lindl. (dendrobium orchid) Dendrobium nobile (family: Orchidaceae) is a owering ornamental plant encompassing nearly 35000 species. The owers are very attractive and appear in various colors and forms. The opened owers mimic bees, wasps, butteries, moths, frogs, lizards, and even humans. Native inhabitants of the Eastern Himalayas (in India) believed that dendrobium owers can cure eye diseases (Uma Devi and others 2009). Gigantel and moscatilin of D. nobile have been reported to exhibit antimutagenic activity and its 2-phenanthrenes to exhibit anticancer activity (Kong and others 2003; Uma Devi and others 2009). Uma Devi and others (2009) used the strip plate method to evaluate the antimicrobial activities of different solvent (methanol, chloroform, and water) extracts of owers and stems of D. nobile against pathogenic bacteria, such as E. coli, B. subtilis, Proteus spp., S. Typhimurium, and S. aureus. The extent of inhibition of oral extracts was high in the aqueous extract than in the other 2 extracts. The authors recorded the inhibition zones as 0.6 to 1.0 mm for ethanol extract, 0.3 to 1.0 mm for chloroform extract, and 0.53 to 1.2 mm for aqueous extract. Also, in aqueous extracts, the
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Hibiscus sabdariffa Linn. (roselle) Hibiscus sabdariffa (family: Malvaceae) is a small shrub native to Africa and is cultivated in parts of Sudan and Eastern Taiwan (Lin and others 2007). The plant parts are used in the treatment of hypertention, pyrexia, and liver disorders (Wang and others 2000; Odigie and others 2003). In vitro and in vivo studies have demonstrated cardio-protective (Odigie and others 2003), hypo-cholesterolemic (Chen and others 2003), antioxidative, and hepatoprotective (Wang and others 2000; Liu and others 2002) properties of the anthocyanins and protocatechuic acid, which were isolated from dried owers of H. sabdariffa. The oral extract (water and ethanol) of H. sabdariffa has been reported to show high inhibitory effects against B. cereus (Hamdan and others 2007). The inhibition zones against B. cereus were 2, 6, and 16 mm and 4, 9, and 12 mm at 1, 2, and 4 mg/mL for water and ethanol extracts, respectively. The authors also noted that as the content of water and ethanol extract increased (from 0.82 to 4.12 mg/mL), a corresponding increase in the inhibition on the growth of B. cereus occurred with complete inhibition (100%) attained at a concentration of 3.45 and 4.12 mg/mL, respectively. Besides, heat treatment at 70 C for 3 min did not signicantly affect the antibacterial activity of H. sabdariffa extract against B. cereus. Jasminum sambac (Arabian jasmine/jasmine ower) Jasminum sambac (family: Oleaceae) originated in India and Burma and is widely grown in Ambouli (Republic of Djibouti) for producing perfume. This plant is a perennial twining shrub (attaining height of 5 to 6 feet) and bearing small, white-colored scented owers. The owers are used ornamentally as well as to decorate hair. Skin care products are also formulated by using the essential oil extracted from the owers. The essential oil of the ower is used to reduce skin inammation, tone the skin, and lift up mood (Abdoul-Latif and others 2010). Extracts of owers are also used to prepare herbal tea decoctions. The oral extract is reported to possess analgesic, anti-inammatory, antidepressant, aphrodisiac, antiseptic, expectorant, sedative, and tonic properties. Besides, owers and plant parts have been reported to have anticancer properties (Houghton and others 2007; Alka and others 2010). Tsai and others (2008) have reported on the inhibitory activities of methanolic extract of the owers against Streptococcus mutans and Streptococcus sanguinis. They adopted the broth microdilution method for evaluating the antimicrobial/inhibitory activities. From their study, they reported the MIC to be 1 mg/mL for S. sanguinis. However, the MIC of the extract for S. mutan was >8 mg/mL, which is an indication of no activity against S. mutans.
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Lonicera japonica Thunb. (honeysuckle) Lonicera japonica (family: Caprifoliaceae) is a native plant of eastern Asia and is widely seen in parts of Japan, Korea, northern and eastern China, and Taiwan. Flower buds of this plant possess anticancer, antimicrobial, and anti-inammatory properties (Zhang and others 2008). Results on the phytochemical screening have reported the presence of iridoid glucosides and polyphenolic compounds in the ower buds (Kakuda and others 2000). Based on the results obtained by the agar well diffusion method, methanol extracts of the ower showed inhibitory activities against B. cereus, S. aureus, and S. anatum with the diameters of inhibition zones ranging from 5.5 to 7.2 mm (Shan and others 2007). On another note, Tsai and others (2008), screening on the methanolic extract of different herbs against growth of S. mutan and S. sanguinis, found MIC of L. japonica to be 4 mg/mL for S. sanguinis, while MIC for S. mutan was >8 mg/mL (no activity). In another study reported by Rahman and Kang (2009), the essential oil of L . japonica ower demonstrated inhibitory activities against L. monocytogenes, B. subtilis, B. cereus, S. aureus, S. enteritidis, S. Typhimurium, E. aerogenes, and E. coli with inhibition zones recorded in the range of 12.1 to 20.3 mm and MIC in the range of 62.5 to 500 g/mL. The authors used the agar disc diffusion and broth dilution assays for the analysis. Their results of a GC-MS analysis showed the essential oil to contain 39 compounds wherein 92.34% of the oil was composed of trans-nerolidol (16.31%), caryophyllene oxide (11.15%), linalool (8.61%), p-cymene (7.43%), hexadecanoic acid (6.39%), eugenol (6.13%), geraniol (5.01%), trans-linalool oxide (3.75%), globulol (2.34%), pentadecanoic acid (2.25%), veridiorol (1.83%),>br/> benzyl alcohol (1.63%), and phenylethyl alcohol (1.25%) as major components. However, antimicrobial activity results on the essential oil did not reveal any effects of the oil against E. coli O157: H7 and P. aeruginosa. Recently, Rhee and Lee (2011) reported the antimicrobial activity of butanol extract from L. japonica ower against 104 clinical isolates of anaerobic bacteria (Bacteroides fragilis, Bacteroides ovatus, Clostridium difcile, C. perfringens, Propionibacterium acnes, and Peptostreptococci) (based on the agar dilution method). The butanol extract showed antimicrobial activity against all the tested bacteria with MIC ranging from 0.032 to 2.0 mg/L. Mentha longifolia L. (horse mint) Mentha longifolia (family: Lamiaceae) is a perennial herb commonly found growing in a hot and humid climate. Mint is widely distributed throughout South Africa, Botswana, Namibia, and Zimbabwe. The rhizomes creep below the ground and the erect owering stems can grow up to 8-m high. The plant bears small white or pale purple owers borne in elongated clusters on the tips of the stems. The entire plant exudes a unique mint aroma. The leaves are the most widely used parts of this plant. Leaf and stem decoctions are prescribed to cure common colds, cough, bronchial ailments, headache, fever, indigestion, atulence, painful menstruation, urinary tract infections, diseases of the gastrointestinal tract, and bleeding problems (http://www.plantzafrica.com/medmonographs/menthlong.pdf, accessed on Jul 25, 2011). In one of the experiments conducted by Pirbalouti and others (2010) on Iranian folklore herbs, the extract and essential oil from owers of M. longifolia have been reported to exhibit strong antibacterial activity against all the tested bacteria (S. aureus, E. coli, P. aeruginosa, and K. pneumoniae) with inhibition zones and MIC values ranging from 9 to 17 mm and 0.156 to 10.00 mg/mL,
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Rumex vesicarius Linn. (bladder dock) Rumex vesicarius (family: Polygonaceae) is a wild edible plant that grows during spring time (Al- Quran 2009). It is native to southwest Asia and North Africa and is cultivated in India, especially in regions of Tripura, West Bengal, and Bihar (Khare 2007). The plant parts are used traditionally in the treatment of various diseases, such as tumors, hepatic diseases, indigestion, constipation, heart diseases, pains, spleen disorder, hiccough, atulence, asthma, bronchitis, dyspepsia, piles, scabies, leucoderma, toothache, nausea, and dysentery. The plant also has cooling, laxative, tonic, antibacterial, analgesic, stomachic, appertizer, diuretic, astringent, purgative, and antispasmodic properties. Besides, this plant is used to reduce biliary disorders and to control cholesterol levels (Elegami and others 2001; Atiqur Rahman and others 2004; Lakshmi and others 2009; Mostafa and others 2011). Antimicrobial activity of different plant parts of this plant against K. pneumoniae, S. pneumoniae, S. pyogenes, S. aureus, E. coli, and P. aeruginosa was performed using the agar disc diffusion method by Mostafa and others (2011). Results of this study demonstrated potential antibacterial activity (K. pneumoniae, Streptococcus pneumonia, S. pyogenes, S. aureus, E. coli, and P. aeruginosa) of the owers extracted in different solvent extracts (petroleum ether, ether, chloroform, methanol, and ethanol). Chemical analysis of ower extracts revealed variations in the presence and amount of active compounds (avonoids, anthraquinones, alkaloids, tannins, sterols and/or triterpenoids, carbohydrates and/or glycosides, chlorides, sulfates, and sublimable substances).
Satureja bachtiarica Bunge. (savory) The genus Satureja (family: Lamiaceae) contains more than 200 species of herbs and shrubs that are widely distributed in the Mediterranean region. Aerial parts of Satureja species are used as avoring agents in a variety of food products as well as for herbal medicine preparations to treat gastrointestinal disorders (Sonboli and others 2004). Pirbalouti and others (2010), by employing agar disc diffusion and serial dilution assays, determined the antimicrobial activities of some of the Iranian folklore herbs against S. aureus, E. coli, P. aeruginosa, and Klebsiella pneumonia. From the results of their screening tests, the ethanolic extract and essential oils of owers of S. bachtiarica showed strong antibacterial activity against all the tested bacteria with the zone of inhibitions ranging from 12 to 23 mm. The MIC values ranged from 0.039 to 10.00 mg/mL. This study showed essential oils to exhibit stronger antibacterial activity than the ethanol extract.
Tamarix gallica L. (French tamarisk) Tamarix gallica (family: Tamaricaceae) is a halophytic tree found growing in natural habitats ranging from coastal regions up to deserts. This plant is known to tolerate a wide range of harsh environmental conditions and can resist abiotic stress, such as salt, high temperature, and dryness (Sa Idana and others 2008; Ksouri and others 2009). In certain parts of Asia, the leaves, owers, and galls of T. gallica are used as therapeutic agents, particularly as anti-inammatory, antidiarrheic, cicatrizing, and antiseptic agents. They are also used for treating leucoderma, spleen trouble, and eye diseases (Ksouri and others 2009). Besides, the plant parts are used as astringent, aperitif, stimulant of perspiration, and diuretic (Sa Idana and others 2008; Ksouri and others 2009). Based on the inhibition zone measured by the disc diffusion assay (Ksouri and others 2009), the methanolic oral extracts (2, 4, and 100 mg/mL) of this plant exhibited antibacterial activities against S. epidermidis, S. aureus, M. luteus, E. coli, and P. aeruginosa. The oral extracts also showed antifungal activity against Candida spp. with inhibition zones of 6 to 15 mm and 6 to 8.66 mm, respectively. The bioactive compounds present in the owers were identied Santolina rosmarinifolia Linn. (green lavender cotton) Santolina rosmarinifolia (family: Asteraceae) is a perennial shrub as phenolic acids (gallic, sinapic, chlorogenic, syringic, vanillic, found in the Iberian peninsula and southern France (Ioannou and p-coumaric, and trans-cinnamic acids) and avonoids (catechin, others 2007). The infusions from ower heads are reported to be isoquercetin, quercetin, apigenin, amentoavone, and avone). used as an antipyretic and have been shown to posses hepatoprotective, antihypertensive, and intestinal anti-inammatory properties Thymus daenensis Celak (thyme) (Novais and others 2004). The genus Thymus (family: Lamiaceae), is a perennial herb that The antimicrobial activity of ower heads and leaves of S. has its origin in the Mediterranean region. Leaves and owers of rosmarinifolia against S. aureus, S. lutea, B. cereus, E. coli, and C. Thymus species are traditionally used in Iran as tonic and herbal albicans was determined by Ioannou and others (2007) based on tea, antitussive, antiseptic, carminative, and a treatment for the agar disc diffusion and broth dilution assays. From their study, common cold. Thymus oil and extracts (leaves and owers) are the antimicrobial activity of essential oil from ower heads of S. widely used by the pharmaceutical, perfume, cosmetic, and food rosmarinifolia at doses of 1, 5, and 10 L was found to be stronger industries (Nejad Ebrahimi and others 2008; Pirbalouti and others than those from the leaves, with inhibition zone diameters rang- 2010).
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Zingiber mioga (Thunb.) Roscoe (Myoga) Zingiber mioga (family: Zingiberaceae), a native to eastern Asia, is widely cultivated in Japan as a perennial herb. The stalks of this plant extend up to 1 m, with slender leaves reaching 30 cm having pine-cone-like ower buds ranging up to 7 to 10 cm in length. In Japan, myogabochi, a traditional food (buns lled with sweetened bean paste) is wrapped with the leaves of this plant to be preserved for a long period. Flower buds have a unique and pungent avor, attributed to the presence of diterpene dialdehyde compound, 2-alkyl-3-methoxypyrazine and (E)-8- -(17)epoxylabd-12-ene-15, 16 dial (myogadial). Due to their pungent avor, the ower buds have been used as a spice and to prepare pickles in Japan (Sakakibara and others 1991; Abe and others 2002). Abe and others (2004) screened for the potential antimicrobial activities of the ower buds against a wide range of bacteria, yeasts, and molds by employing the agar disc diffusion assay. The results of their study revealed ethyl acetate extracts of ower buds to exhibit appreciable antimicrobial activity with an inhibition zone of 8 mm, while the methanol extract showed minimal activity with an inhibition zone of 2 mm. Additionally, MICs of the 3 diterpene dialdehydes (myogadial, galanal A, and galanal B) isolated from the ethyl acetate extract were measured using the serial dilution method. From the results, myogadial, galanal A, and galanal B were found to be effective against Gram-positive bacteria and yeast with myogadial (MIC = 25 to 125 g/mL) showing higher activity compared to galanal A and B (MIC = 200 to 500 g/mL). The reason for the antimicrobial activity has been attributed by the authors to the presence of galanal A and B that were present in the 1, 6 positions of the aldehyde groups, with the introduction of a hydroxyl group in their molecules.
Phenolic acids and quinones Phenolic compounds as phenolic acids (gallic, sinapic, chlorogenic, syringic, vanillic, p-coumaric, and trans-cinnamic acids) are also found in ower extracts (Ksouri and others 2009). Quinones are highly reactive compounds that have aromatic rings with 2 ketone substitutions. The antimicrobial activity of quinones involve forming of complex with proteins (surfaceexposed adhesins), cell wall polypeptides, and membrane-bound enzymes, leading to inactivation of function of the proteins (Stern and others 1996; Cowan 1999). Besides, quinones are capable of rendering a substrate unavailable to microorganisms, thus inhibiting their growth. Mostafa and others (2011) described the presence of anthraquinones in various extracts of R. vesicarius owers, which served as one of the antimicrobial compounds against the tested microorganisms (K. pneumonia, S. pneumoniae, S. pyogenes, S. aureus, E. coli and P. aeruginosa). In one of the experiments conducted by Bhalodia and others (2011) on hydro-alcohol and chloroform extracts of C. stula owers, anthraquinones present in the extracts was found to exhibit rich antimicrobial activities, which were found to be active against some sensitive bacteria and fungi (S. aureus, S. pyogenes, E. coli, P. aeruginosa, A. niger , A. clavatus, and C. albicians). Tannins Tannins are a group of polymeric phenolic compounds widespread in plants. Tannins are known to exhibit astringent properties and are synthesized by condensation of avan derivatives or polymerization of quinone units (Haslam 1996; Cowan 1999). Tannins form complex with microbial adhesins, enzymes, and cell envelope transport proteins, leading to inactivation of these proteins and inhibition of microbial growth (Haslam 1996; Stern and others 1996). Scientic evidences showed tannins to be effective against lamentous fungi, yeasts, and bacteria (Brownlee and others 1990; Scalbert 1991; Cowan 1999). Some examples of owers with presence of high tannin include: Allium spp. (Chehregani and others 2007), C. stula (Bhalodia and others 2011), E. elatior (Lachumy and others 2010) and R. vesicarius (Mostafa and others 2011). Terpenoids and essential oils Essential oils are secondary metabolites containing a mixture of compounds that are based on 5 carbon isoprene structure (terpenes) occurring as diterpenes, triterpenes, tetraterpenes (C20, C30, and C40), hemiterpenes (C5), and sesquiterpenes (C15) (Cowan 1999). The antimicrobial activity of terpenes involves
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Phenolics Among the various phenolic compounds, avonoids are found abundantly in plant-derived foods (Denny and Buttriss 2007). Flavonoids (consisting of a central 3-ring structure), are major phenolic compounds that play a pivotal role in plants, such as protection against UV, pigmentation, stimulation of nitrogen xing nodules, and disease resistance (Pierpoint 2000; Denny and Buttriss 2007). This group of compounds can occur as glycosides too. Flavonoids are known to exhibit rich antioxidant, anticarcinogenic, and anti-inammatory properties. Besides, avonoids are known to possess antimicrobial activities due to their ability to form complexes with extracellular and soluble proteins and microbial cell wall (Tsuchiya and others 1996; Cowan 1999; Grotewold 2006).
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Glycosides Glycosides are composed of a variety of secondary metabolites bound to a mono- or oligosaccharide or to uronic acid. The part of saccharide or uronic acid is known as glycone, and the backbone is known as aglycone. Cardiac glycosides, cyanogenic glycosides, glucosinolates, saponins, and anthraquinone glycosides, being different in their aglycone structures, are the main groups of glycosides (Bernhoft 2010). Investigations carried out on the owers of C. stula, C. Juncea, and R. vesicarius have clearly demonstrated the presence of glycosides in their extracts (Chouhan and Singh 2010; Bhalodia and others 2011; Mostafa and others 2011). Alkaloids Alkaloids are heterocyclic, nitrogen-containing compounds, with potential clinical properties. Alkaloids have bitter taste and are present in threshold level in plants (Bernhoft 2010). Flowers of C. juncea and R. vesicarius have been reported to contain alkaloids (Chouhan and Singh 2010; Mostafa and others 2011). Even though a wide range of bioactive compounds might be present in owers, still there is a lack of detailed investigations carried out on these aspects. These needs to be explored further to conrm the antimicrobial activities exhibited.
Acknowledgments
The authors gratefully acknowledge anonymous referees and Scientic Editor (Prof. Dr. Manfred Kroger) for comments and constructive suggestions provided for improving the quality of this manuscript. First author thanks Inst. of Postgraduate Studies, Univ. Sains Malysia for the fellowship provided. Individual research fund provided as an RU grant (Nr 1001/PTEKIND/814139,USM) for the corresponding author is also gratefully acknowledged.
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