Abstract
Drug resistance to human infectious diseases caused by pathogens lead to premature deaths through out the world. Plants are sources for wide variety of drugs used for treating various diseases. Systematic screening of medicinal plants for the search of new antimicrobial drug candidates that can inhibit the growth of pathogens or kill with no toxicity to host is being continued by many laboratories. Here we review the phytochemical investigations and biological activities of Meliaceae. The mahogany (Meliaceae) is family of timber trees with rich source for limonoids. So far, amongst the different members of Meliaceae, Azadirachta indica and Melia dubia have been identified as the potential plant systems possessing a vast array of biologically active compounds which are chemically diverse and structurally complex. Despite biological activities on different taxa of Meliaceae have been carried out, the information of antibacterial and antifungal activity is a meager with exception to Azadirachta indica. Together we provide new insights of Meliaceae members demonstrating as a potential source as antimicrobial agents using in vitro studies.
Limonoids; Flavonoids; Antibacterial; Antifungal activity
Introduction
World wide, infectious disease is the number one cause of death accounting for approximately one-half of all deaths in tropical countries. Plants constitute one of the major raw materials of drugs for treating various human diseases. The modern society has been interested in drugs of natural origin due to their harmonious nature with our biological system (Amalraj, 1983Amalraj, V.A., 1983. Secondary Plant Constituents. Sci. Rep., June issue, CSIR, Oxfordand IBH Publishing Co. Pvt. Ltd., New Delhi, Calcutta.). It is reported that 41% prescriptions in USA and 50% in Europe contain constituents from natural products which shows that the trend of using natural products is getting increased. Scientific research on medicinal plants relies on identification of the active principles in the plants; scientific examination of the remedies which lead to standardization and quality control of products to ensure their safety. It is after such evaluations that they can be approved for use in the primary health care. Such research activities could also lead to the development of new drugs as in the past (Farnsworth et al., 1985Farnsworth, N.R., Akerele, O., Bingel, A.S., Soejarto, D.D., Guo, Z., 1985. Medicinal plants in therapy. Bull. World Health Organ. 63, 965–981.; Farnsworth, 1988Farnsworth, N.R., 1988. Screening plants for new medicines. In: Wilson, E.O. (Ed.), Biodiversity. National Academy Press, Washington, DC, pp. 83–97.). Phytochemical tests have been performed in about 5000 species and nearly 1100 species are extensively exploited in Ayurvedic, Unani and Allopathic medicines. In fact active plant extracts screening programs continue to end always with new drug discoveries.
In order to find new sources of plant drugs, number of plants has been screened for wide range of biological activity in various research institutions. Plant based antimicrobials represent a vast untapped source for medicines by possessing enormous therapeutic potential. They are effective in the treatment of infectious diseases while simultaneously mitigating many of the side effects that are often associated with synthetic antimicrobials. Although, a number of antibiotics are widely used in medicine, the search for antimicrobial substances from plants will continue as better and safer drugs to combat bacterial and fungal infections are still needed, because of their biodegradable nature and being relatively safer for human beings and non-target organisms in the environment. Extensive survey of the flora has been undertaken to search for potential plant extracts, which could be used in the management of agriculture and household pests. In order to study possible applications of extracts or compounds derived from extracts, methods to screen for biological activities and separation techniques to isolate the active principles have to be established. Nearly 80% of the world's population relies on traditional medicines for primary health care, most of which involve the use of plant extracts (Sandhya et al., 2006Samy, R.P., Ignacimuthu, S., 1998. Antibacterial activity of different extracts of Azadirachta indica Juss. Neem. J. Zoo. 18, 71–75.). Almost 95% of the prescriptions are plant based in the traditional systems of Unani, Ayurveda, Homoeopathy and Siddha (Satyavati et al., 1987Sandanasamy, J., Nour, A.H., Tajuddin, S.N.B., Nour, A.H., 2013. Fatty acid composition and antibacterial activity of neem (Azadirachta indica) seed oil. Open Conf. Proc. J. 4, 43–48.).
The mahogany (Meliaceae) family comprises more than fifty genera with about 1400 species (Nakatani et al., 2001Nakatani, M., Abdelgaeil, S.A.M., Kassem, S.M.I., Takezaki, K., Okamura, H., Iwagawa, T., Doe, M., 2002. Three new modified limonoids from Khaya senegalensis. J. Nat. Prod. 65, 1219–1221.) is distributed in tropical and subtropical regions. The family is represented by seventeen genera and 72 species of which twelve species and two varieties endemic in India. Approximately 18% are endemic to peninsular India. From 19th century up to the present time, the mahoganies have been the most important species for the development of the forest industry in Asia, tropical Africa and Latin America. Many species of this family were used in traditional medicine for treatment of various diseases and also in pest control. Here we review the phytochemical investigations and biological activities of Meliaceae. Together we provide insights of Meliaceae members demonstrating as a potential source as antimicrobial agents using in vitro studies. Till to date there is no review published on the phytochemical constituents and their antimicrobial properties of Meliaceae. Hence our review aims to coherently unite results obtained from various published investigations on this important family. Here we address the important phytochemical constituents of Meliaceae and plants that have been investigated for their antimicrobial potential other than A. indica from Meliaceae.
Phytochemical studies of Meliaceae
Various classes of chemical constituents were isolated from different parts of meliaceous members. Chemically, the Meliaceae is characterized by synthesis of modified triterpenes known as limonoids. Over 300 limonoids have been isolated to date and they are more diverse and abundant in this particular family than in any other family. Several triterpenoidal derivatives were also isolated from different genera of Meliaceae. Amongst different members of Meliaceae, Azadirachta indica had been extensively studied for its chemicals. Limonoids are secondary metabolites produced in plants found in the order Rutales. Over 300 limonoids have been isolated to date (Taylor, 1986Tane, P., Akam, M.T., Tsopmo, A., Ndi, C.P., Sterner, O., 2004. Two lab danediterpenoids and a seco-tetranortriterpenoid from Turreanthus africanus. Phytochemistry 65, 3083–3087.; Champagne et al., 1992Champagne, D.E., Koul, D.E., Isman, M.B., Scudder, G.G.E., Towers, G.H.N., 1992. Biological activity of limonoids from the Rutales. Phytochemistry 31, 377–394.) and their production is confined to plants in the order Rutales. In particular, they are characteristic members of the family Meliaceae where they are diverse and abundant (Taylor, 1981Tanaka, T., Koyano, T., Kowithayakorn, T., Fujimoto, H., Okuyama, E., Hayashi, M.,Komiyama, K., Ishibashi, M., 2001. New multiflorane-type triterpenoid acids from Sandoricum indicum. J. Nat. Prod. 64, 1243–1245.; Connolly, 1983Connolly, J.D., 1983. In: Waterman, P.G., Grundon, M.F. (Eds.), Chemistry and Chemical Taxonomy of the Rutales. Academic Press, New York, p. 175.) than in any other family and less frequently in the families Rutaceae and Cneoraceae.
Limonoids are described as modified triterpenes, having a 4,4,8-trimethyl-17-furanyl steroid skeleton. The term limonoids was derived from limonin, the first tetranortriterpenoid obtained from citrus bitter principles (Roy and Saraf, 2006Rogers, L.L., Zeng, L., Mc Laughlin, J.L., 1998. Volkensinin – a new limonoid from Melia volkensii. Tetrahedron Lett. 39, 4623–4626.). The effect of ring structure and chemical oxidation state parameters is a focus of why limonoids exhibit activity against insect herbivores. Arrangements of subgroups and ring structures within this basic building block provide a host of characteristics that have generated interest in this plant product. These characteristics include insecticidal, insect growth regulation, insect antifeedant, and medicinal effects to animals and humans such as antibacterial, viral, and antifungal properties. Of recent great interest, limonoid's possible anticarcinogenic properties are being explored. Of special interest to countries in tropical locations is the antimalarial activity attributed to tropical Meliaceae extracts and gendunin (1) derivatives. Previous investigations from various plant parts of Meliaceae led to the isolation of tetranortriterpenoids with a modified furan ring such as febrifugin (2)(Rao et al., 1978Randrianarivelojosia, M., Kotsos, M.P., Mulholland, D.A., 1999. A limonoid from Neobeguea mahafalensis. Phytochemistry 52, 1141–1143.) methyl angolensate (3), luteolin-7-O-glucoside (4), deoxyandirobin (5) from the bark (Ambaye et al., 1971Ambaye, R.Y., Indap, M.A., Panse, T.B., 1971. Identification of methyl angolensate inthe bark of Soymida febrifuga (Roxb.) A. Juss. Curr. Sci. India 7, 158–159.; Adesida and Taylor, 1972Adesida, G.A., Taylor, D.A.H., 1972. Extractives from Soymida febrifuga. Phytochem-istry 11, 1520–1524.; Purushothaman and Chandrasekharan, 1974Pupo, M.T., Vieira, P.C., Fernandes, B., Fatima Das, M., Da Silva, G.F., Rodrigues,E., 1997. Androstane e pregnane 2-beta, 19-hemiketal steroids from Trichilia claussenii. Phytochemistry 45, 1495–1500.; Purushothaman et al., 1977Pupo, M.T., Vieira, P.C., Fernandes, B., Fatima Das, M., Da Silva, G.F., Rodrigues,E., 1997. Androstane e pregnane 2-beta, 19-hemiketal steroids from Trichilia claussenii. Phytochemistry 45, 1495–1500.).
Tetranortriterpenoids febrifugin (2) (Rao et al., 1978Randrianarivelojosia, M., Kotsos, M.P., Mulholland, D.A., 1999. A limonoid from Neobeguea mahafalensis. Phytochemistry 52, 1141–1143.) and febrinins A and B (6) (Rao et al., 1979Rao, M.M., Gupta, P.S., Krishna, E.M., Singh, P.P., 1979. Constituents of heartwood of Soymida febrifuga – isolation of flavonoids. Ind. J. Chem. 17B, 178–180.) together with the flavonoids naringenin (7), quercetin (8), myricetin (9)and dihydromyricetin (10) from the heartwood (Rao et al., 1979Rao, M.M., Krishna, E.M., Guptam, P.S., Singh, P.P., 1978. A new tetranortriterpenoid isolated from the heartwood of Soymida febrifuga. Ind. J. Chem. 16B, 823–825.).
Seed oil containing linolenic, linoleic, oleic, palmitic and stearic acid, lupeol and sitosterol (Yoganarasimhan, 1996Yin, J.L., Di, Y.T., Fang, X., Liu, E.D., Liu, H.Y., He, H.P., Li, S.L., Li, S.F., Hao, X.J., 2011. Tabulvelutin A, the first 19-nor limonoid with unprecedented ring system from Chukrasia tabularis var. velutina. Tetrahedron Lett. 52, 3083–3085.). Leaves were found to contain quercetin-3-O-└-rhamnoside and 3-O-rutinoside (Rastogi and Mehrotra, 1993Ragasa, C.Y., Torres, O.B., Bernardo, L.B., Mandia, E.H., Don, M.J., Shen, C.C., 2013. Glabretal-type triterpenoids from Dysoxylum mollissimum. Phytochem. Lett. 6, 514–518.).
In view of the characteristic occurrence of the gedunin nucleus in the Meliaceae, the name meliacin has been proposed for this nucleus (Bevan et al., 1963Bevan, C.W.L., Powell, J.W., Taylor, D.A.H., 1963. West African timbers. Part VII. Anthothecol, an extractive from Khaya anthotheca. J. Chem. Soc., 983–993.). Compounds which may arise from closely similar biogenetic routes have also been isolated from the related families Rutaceae and Simarubaceae (Arigoni et al., 1960Arigoni, D., Barton, D.H.R., Bernasconi, R., Djerassi, C., Mills, J.S., Wolff, R.E., 1960. Theconstituents of dammarenolic and nyctanthic acid. J. Chem. Soc., 1900–1905.; Narayanan et al., 1964Nanduri, S., Banstola, P., 1995. Neeflone, a new tetranortriterpenoid from the flowers of Azadirachta indica A. Juss (Meliaceae). Ind. J. Chem. 34, 1019–1021.). It has been proposed that the Meliaceae compounds are derived biogenetically from an apo-euphol type triterpene in which the side chain has been oxidized leaving a furan ring (Arigoni et al., 1960Arigoni, D., Barton, D.H.R., Bernasconi, R., Djerassi, C., Mills, J.S., Wolff, R.E., 1960. Theconstituents of dammarenolic and nyctanthic acid. J. Chem. Soc., 1900–1905.). Possessing a reduced furan ring, flindissol is structurally midway between epo-euphol and the meliacins, and indicates a biochemical relationship between the two families. This interference is strengthened by the occurrence of a coumarin, a characteristic of the Rutaceae, in Ekbergia senegalensis (Meliaceae). It is hoped that elucidation of the structures of the other meliacins will reveal features giving more information about the biochemical relationships of these compounds, as well as making available further taxonomic criteria in this important family.
Various classes of chemical constituents were isolated from different parts of meliaceous members (Box 1). Amongst the different members of Meliaceae, Azadirachta indica and Melia dubia have been identified as the potential plant systems possessing a vast array of biologically active compounds, which are chemically diverse and structurally complex. It seems that other members of this family are tested for secondary metabolites and bioactivity besides multiplication, overcoming physiological barriers.
Antimicrobial activity of Meliaceae
One of the major triumphs of medical science in the millennium has been the virtual eradication of many infectious diseases by the use of specific antimicrobial agents. Two important discoveries marked the beginning of a new era in chemotherapy. First discovery in 1935 curative discovery and development of the sulfonamide on Streptococcal infection. Second important pharmacokinetic property of the antibiotics quite varied, as are their antimicrobial spectra and mechanisms of action. Although, a number of antibiotics are widely used in medicine, the search for antimicrobial substances from plants will continue as better and safer drugs to combat bacterial and fungal infections are still needed, because of their biodegradable nature and being relatively safer for human beings and non target organisms in the environment. Plant extracts that inhibit pathogenic microorganisms without harming the host may have potential use as therapeutic agents. The susceptibility of a microorganism to antibiotics and other chemotherapeutic agents can be determined by the different methods available like tube-dilution, Paper-disk-plate, cylinder and well methods, single disk method and agar overlay method. The screening of large numbers of bacteria and fungi with various antibiotics and synthesized drugs requires simple techniques that can be used with several samples at the same time. Disk diffusion method for susceptibility testing currently recommended by the FDA is a slight modification of the procedure developed by Bauer et al. (1966)Bauer, A.W., Kirby, M.D.K., Sherris, J.C., Turck, M., 1966. Antibiotic susceptibility testing by a standardized single disk method. Am. J. Clin. Pathol. 45,493–496.. Different parts of meliaceous members were screened for the antibacterial and antifungal activity (Box 2).
Ethyl acetate extracts of Chukrasia tabularis leaves inhibited the growth of microorganisms like Staphylococcus aureus, Escherichia coli, Proteus vulgaris, Klebsiella pneumoneae, Aspergillus fumigatus and Pseudomonas aeruginosa (Nagalakshmi et al., 2001Nagalakshmi, M.A.H., Thangadurai, D., Rao, D.M., Pullaiah, T., 2001. Phytochemical and antimicrobial study of Chukrasia tabularisleaves. Fitoterapia 72, 62–64.). Jayasinghe et al. (2002)Jayasinghe, U.L.B., Jayasooriya, C.P., Bandara, B.M.R., Ekanayake, S.P., Merlini, L., Asante, G., 2002. Antimicrobial activity of some Sri Lankan Rubiaceae and Meliaceae. Fitoterapia 73, 424–427. screened the antimicrobial activity of two Meliaceae members like Agalia congylos and Munronia pumila. According to them the methanol, n-hexane and dichloromethane extracts of leaves, bark and stem displayed the wide spectrum of antimicrobial activity against Aspergillus, Saccharomyces, Ustilago, Eschericia, Micrococcusand Bacillus species. Antibacterial activity of methanol and acetone flower extracts of Azadirachta indica by disk assay on most sensitive organisms like Staphylococcus aureus, Listeria monocysgenes, Escherichia coli, Bacillus cereus and Salmonella infantis were tested by Alzoreky and Nakahara (2003)Alzoreky, N.S., Nakahara, K., 2003. Antibacterial activity of extracts from some edible plants commonly consumed in Asia. Int. J. Food Microbiol. 80, 223–230.. Aladesanmi and Odediran (2000)Aladesanmi, A.J., Odediran, S.A., 2000. Antimicrobial activity of Trichilia heudelotti leaves. Fitoterapia 71, 179–182. stated that Trichlia heudelotti leaves can be regarded as having moderate antibacterial and antifungal activities determined by the cup plate method using n-hexane, ethyl acetate, methanol extracts and some isolated compounds. Chowdhury et al. (2003a)Bauer, A.W., Kirby, M.D.K., Sherris, J.C., Turck, M., 1966. Antibiotic susceptibility testing by a standardized single disk method. Am. J. Clin. Pathol. 45,493–496. reported that petrol ether, dichloromethanol and methanol extracts along with siderin of two Meliaceae medicinal plants, Toona ciliata and Amoora rohituka (stem bark) exhibited significant antibacterial activity and mild antifungal effect.
Although several aspects of biological activity on different taxa of Meliaceae have been carried out, the information of antibacterial and antifungal activity is a meager excepting that of Azadirachta indica. Samy and Ignacimuthu (1998)Samy, R.P., Ignacimuthu, S., 1998. Antibacterial activity of different extracts of Azadirachta indica Juss. Neem. J. Zoo. 18, 71–75. reported that when antibacterial activity of different crude extracts of seed kernel, seed coat and leaves of Azadirachta indica were tested against Escherichia coli, Pseudomonas aerogenes, Klebsiella aerogenes and Proteus vulgaris, only the seed kernel extracts was found to show significant antibacterial activity. Another interesting feature reported was inhibitory action of seed and leaf extracts of Azadirachta indica on fungi such as Candida albicans, C. tropicalis, Neisseria gonorrhoeae and the multi drug resistant Staphylococcus aureus (Talwar et al., 1997Talwar, G.P., Raghuanshi, P., Misra, R., Mukerjee, S., Shah, S., 1997. Plant immunomodulators for termination of unwanted pregnancy and for contraception and reproductive health. Immunol. Cell Biol. 75, 190–192.). Jayasinghe et al. (2002)Jayasinghe, U.L.B., Jayasooriya, C.P., Bandara, B.M.R., Ekanayake, S.P., Merlini, L., Asante, G., 2002. Antimicrobial activity of some Sri Lankan Rubiaceae and Meliaceae. Fitoterapia 73, 424–427. screened Srilankan Meliaceae plants for antibacterial and antifungal activity.
Triterpenoids are an important group of constitutive defense substances present at sufficient concentrations to ward off potential plant pathogenic fungi (Grayer and Harborne, 1994Grayer, R.J., Harborne, J.B., 1994. A survey of antifungal compounds from higherplants, 1982–1993. Phytochemistry 37, 19–42.). Triterpenoids from the family Meliaceae, in particular, are highly diversified in structure and have been extensively studied for their insect antifeedant and growth regulating activities (Champagne et al., 1992Champagne, D.E., Koul, D.E., Isman, M.B., Scudder, G.G.E., Towers, G.H.N., 1992. Biological activity of limonoids from the Rutales. Phytochemistry 31, 377–394.). Extracts from seeds of the neem tree Azadirachta indica containing triterpenoidal compounds are known to be effective against plant pathogenic fungi (Khan et al., 1974Khan, M.W., Alam, M.M., Saxsena, S.K., 1974. Effect of water-soluble fractions of oil cakes and bitter principles of neem on some fungi and nematode. Acta Bot. Indica. 2, 120–128.; Singh et al., 1980Singh, U.P., Singh, H.B., Singh, R.B., 1980. The fungicidal effect of neem (Azadrichta indica) extracts on some soilborne pathogens of gram (Cicer arietinum). Mycologia 72, 1077–1093.; Locke, 1995Locke, J.C., 1995. Fungi in the neem tree sources of unique natural products for integrated pest management, medicine, industry and other purposes. VCH, Weinheim, Germany, pp. 118–127.; Coventry and Allan, 1996Carvalho, D.D., Alves, E., Barbosa Camargos, R., Oliveira, D.F., Soares Scolforo, J.R., de Carvalho, D.A., Sâmia Batista, T.R., 2011. Plant extracts to control Alternaria alternata in murcott tangor fruits. Rev. Iberoam Micol. 28, 173–178.; Govindachari et al., 1998Govindachari, T.R., Suresh, G., Gopalakrishnan, G., Banumathy, B., Masilamani, S.,1998. Identification of antifungal compounds from the seed oil of Azadirachta indica. Phytoparasitica 26, 106–109.; Steinhauer, 1999Steinhauer, B., 1999. Possible ways of using the neem tree to control phytopathogenic fungi. Plant Research and Development, Hamburg, v. 50, vol. 50.,pp. 83–92.). Antifungal triterpenoids of the Meliaceae include four meliacins from Chisocheton paniculatus (Bordoloi et al., 1993Bordoloi, M., Saikia, B., Mathur, R.K., Goswami, B.N., 1993. A meliacin from Chisocheton paniculatus. Phytochemistry 34, 583–584.) and nimonol and isomeldenin from Azadirachta indica (Suresh et al., 1997Takeya, K., Qiao, Z., Hirobe, C., Itokawa, H., 1996. Cytotoxic azadirachtin-type limonoids from Melia azedarach. Phytochemistry 42, 709–712.).
A number of limonoids have been reported from the genus Swieteniawith structures assigned on the basis of spectral data (Kadota et al., 1990Kadota, S., Marpaung, L., Kuchi, T.K., Ekimoto, H., 1990. Constituents of the seeds of Swietenia mahagoni Jacq. Isolation, structures and proton and carbon-13 nuclear magnetic resonance signal assignments of new tetranortripenoids related to swietenine and swietenolide. Chem. Pharm. Bull. 38, 639–651.). Seven limonoids from methanolic extract of the seeds of Swietenia mahogani were isolated by Govindachari et al. (1999b)Govindachari, T.R., Suresh, G., Banumathy, B., Masilamani, S., Gopalakrishnan, G., Krishna kumara, G.N., 1999b. Antifungal activity of some B,D-seco limonoids from two meliaceous plants. J. Chem. Ecol. 25, 923–933.. Triterpenoids (B,D-seco limonoids) from S. mahogani and Khaya senegalensis were evaluated for their antifungal activities (Govindachari et al., 1999bGovindachari, T.R., Suresh, G., Banumathy, B., Masilamani, S., Gopalakrishnan, G., Krishna kumara, G.N., 1999b. Antifungal activity of some B,D-seco limonoids from two meliaceous plants. J. Chem. Ecol. 25, 923–933.). Methyl angolensate and luteolin-7-O-glucoside obtained from ethyl acetate extracts of Soymida febrifuga root callus had an antibacterial effect against Bacillus subtilis and Salmonella typhimurium, respectively. In addition to that methyl angolensate had an anti-fungal activity against Aspergillus niger while luteolin-7-O-glucoside inhibited Alternaria alternata (Chiruvella et al., 2007Chiruvella, K.K., Mohammed, A., Dampuri, G., Ghanta, R.G., Raghavan, S.C., 2007. Phytochemical and antimicrobial studies of methyl angolensate and luteolin-7-O-glucoside isolated from callus cultures of Soymida febrifuga. IJBS 3, 269–278.).
Conclusion
Here we compiled the phytochemical and antimicrobial studies in taxa belong to the most important medicinal family Meliaceae, which might be effective in controlling infectious diseases. Nonetheless, the effectiveness of these phytochemicals needs to be validated in vivo for further investigation. Among the Meliaceae members, the genus Aglaia, Azadirachta, Dysoxylum, Swietenia, Trichilia have been more explored for the phytochemical screening where as Azadirachta, Swietenia, Trichilia have been more explored for their antimicrobial properties. Our critical analysis of published research data shows that most of the antimicrobial screening was carried out using plant crude extracts which is not much useful for further drug development. As these extracts contain many compounds along with the active compounds may cause side or toxic effects. Hence future research should be focused on the isolation and identification of active compounds with antimicrobial activity rather than simply screening the plant crude extracts. In addition research should take in depth studies to know the mechanism of action of drug so that it is beneficial for drug discovery and development. This review stands as a readymade map for phytochemical constituents and antimicrobial activities of Meliaceae family for the future researchers dealing with Meliaceae members.
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1
These authors equally contributed to this work.
Acknowledgements
We thank Gayathri Dampuri for critical reading and help. The authors are highly grateful to the UMK for their logistical support under Grant No. R/SGJP/A07.00/00710A/001/2012/000081.
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Publication Dates
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Publication in this collection
Jan-Feb 2015
History
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Received
09 July 2014 -
Accepted
03 Nov 2014