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Journal on New Biological Reports 2(2): 142-162 (2013) ISSN 2319 – 1104 (Online) Glimpses of antimicrobial activity of fungi from World Kiran R. Ranadive1* Mugdha H. Belsare2, Subhash S. Deokule2, Neeta V. Jagtap1, Harshada K. Jadhav1 and Jitendra G. Vaidya2 1 2 Waghire College, Saswad, Pune – 411 055, Maharashtra, India Department of Botany, University of Pune, Pune (Received on: 17 April, 2013; accepted on: 12 June, 2013) ABSTRACT As we all know that certain mushrooms and several other fungi show some novel properties including antimicrobial properties against bacteria, fungi and protozoan’s. These properties play very important role in the defense against several severe diseases caused by bacteria, fungi and other organisms also. In the available recent literature survey, many interesting observations have been made regarding antimicrobial activity of fungi. In particular this study shows total 316 species of 150 genera from 64 Fungal families (45 Basidiomycetous and 21 Ascomycetous families {6 Lichenized, 15 Non-Lichenized and 3 Incertae sedis)} are reported so far from world showing antibacterial activity against 32 species of 18 genera of bacteria and 22 species of 13 genera of fungi. This data materialistically adds the hidden potential of these reported fungi and it also clears the further line of action for the study of unknown medicinal fungi useful in human life. Key Words: Fungi, antimicrobial activity, microbes INTRODUCTION In recent in vitro study, extracts of more than 75 percent of polypore mushroom species surveyed showed antimicrobial activity and 45 percent of 204 mushroom species (polypore and gilled mushrooms alike) inhibited the growth of a wide variety of microorganisms (Suay et al. 2000). But after extensive literature survey a very significant observation showed that total 316 species of 150 genera from 64 fungal families [45 Basidiomycetous and 21 Ascomycetous families {6 Lichenized, 15 Non-Lichenized and 3 Incertae sedis}] are reported so far from world showing antibacterial activity against 32 species of (18 genera) bacteria and 22 species (13 genera) of fungi. The list of total species with families and genera is provided which gives the idea in details about the species involved in the antimicrobial activities from world. (Table 1 & 2, Fig. 1&2) As far as the organisms used for the antimicrobial activities are concerned, there are 54 species of organisms including bacteria and fungi were observed. From these organisms bacterial families like Bacillaceae, Enterobacteriaceae and Fungi and animals are more closely related to one another than either is to plants, diverging from plants more than 460 million years ago (Redecker 2000). Diseases of plants typically do not afflict humans whereas diseases of fungi do (Martin 2001). Since humans (animals) and fungi share common microbial antagonists such as Escherichia coli, Staphylococcus aureus and Pseudomonas aeruginosa, humans can benefit from the natural defensive strategies of fungi that produce antibiotics to fight infection from microorganisms. Hence, it is not surprising our most significant antibacterial antibiotics have been derived from fungi. The fact that mushrooms can have both anti-viral and anti-bacterial properties, with low cytotoxicity to animalian hosts, underscores their usefulness as natural sources of medicine. (Stamets 2002). Gilled mushrooms (Order Agaricales) had more species with antifungal activity than polypores (Suay et al. 2000). *Corresponding author: ranadive.kiran@gmail.com 142 Kiran R. Ranadive et al., 2013 Staphylococcaceae are found to be more dominantly used for the testing purpose (Table 4, Figure 3). When the species wise dominance is seen for the antibacterial activity of fungi, Polyporaceae, Agaricaceae Hymenochaetaceae, Tricholomataceae, Fomitopsidaceae, Meruliaceae are found more dominantly used for the same respectively (Table 3). Table 1. List of family, species, genera of fungi and lichens showing the antimicrobial activity against bacteria and fungi Fungal Group Basidiomycetes Family Amanitaceae Genera Amanita Species Amanita foetens Amanita muscaria Amanita cesarae Physalacriaceae Armillaria Armillaria mellea Armillaria ostoyae Armillaria tabescens Cyptotrama asprata Rhodotus palmatus Strobilurus tenacellus Oudemansiella canarii Oudemansiella longipes Oudemansiella mucida Oudemansiella sp. Agaricus bisporus Agaricus campestris Agaricus langei Agaricus nigrescentibus Agaricus porosporus Agaricus trinitatensis Leucoagaricus gongylophorus Leucoagaricus pudicus Leucoagaricus cinerascens Leucocoprinus longistriatus Macrolepiota rhacodes Podaxis pistillaris Chlorolepiota sp. Coprinus episcopalis Coprinus cinereus Lepiota sp. Bovista plumbea Crucibulum laeve Cyptotrama Rhodotus Strobilurus Oudemansiella Agaricaceae Agaricus Leucoagaricus Macrolepiota Podaxis Chlorolepiota Coprinus Lepiota Bovista Crucibulum 143 Few References Mustafa 2006; Yamac & Bilgili 2006; Mustafa 2006; Dighe & Agate 2000 Donnelly et al. 1985, 1986; Yamac & Bilgili 2006, Mustafa 2006, Vahidi & Namjoyan 2004, Ahmed Imtiaj & Tae-Soo Lee, Imtiaj & Lee 2007 Ndyetabura et al. 2010; Theonest 2010; Yamac & Bilgili 2006; Mustafa 2006, Dighe & Agate 2000; Banarji & Hariprasad 2011; Akyuz et al. 2010; Banerji & Hariprasad 2011; Surekha et al. 2011; Imtiaj & Lee 2007; Akyuz et al. 2010 Journal on New Biological Reports 2(2): 142-162 (2013) Table 1. contd..... Lycoperdon Calvatia Cyphellaceae Chondrostereum Entolomataceae Claudopus Fistulinaceae Fistulina Tricholomataceae Clitocybe Lepista Tricholoma Collybia Leucopaxillus Lepista Pseudoclitocybe Marasmiaceae Crinipellis Marasmius Lentinula Nothopanus Coniophoraceae Inocybaceae Coniophora Crepidotus 144 Lycoperdon echinatum Lycoperdon giganteum Calvatia craniiformis Chondrostereum purpureum Claudopus byssisedus Fistulina sp. Clitocybe nebularis Clitocybe geotropa Lepista nuda Tricholoma auratum Tricholoma fracticum Tricholoma lobayense Tricholoma portentosum Collybia butyracea Collybia dryophila Collybia fusipes Leucopaxillus giganteus Leucopaxillus lepistoides Lepista luscina Lepista nuda Lepista personata Pseudoclitocybe expallens Crinipellis stipitaria Marasmius allocystis Marasmius androsaceus Marasmius bellus Marasmius cladophyllus Marasmius corbariensis Marasmius oreades Marasmius quercophilus Lentinula edodes Nothopanus hygrophanus Coniophora arida Crepidotus variabilis Pearce 1996 Dighe & Agate 2000 Bose 1946; Bannur et al. 1967 Yamac & Bilgili 2006; Mustafa 2006; Dighe & Agate 2000; B Florey et al. 1949 Rosa et al 2003 Iakovlev 2003 Mtui 2012 Kiran R. Ranadive et al., 2013 Table 1. contd..... Pleurotellus Niaceae Cyphellopsis Strophariaceae Agrocybe Gymnopilus Hypholoma Pholiota Psilocybe Stropharia Pleurotaceae Hohenbuehelia Pleurotus Russulaceae Lactarius Russula 145 Pleurotellus hypnophilus Cyphellopsis anomala Agrocybe semiorbicularis Gymnopilus aureobrunneus Gymnopilus areolatus Gymnopilus chrysopellus Hypholoma fasciculare Pholiota destruens Pholiota carbonaria Pholiota adiposa Psilocybe semilanceata Psilocybe venezuelana Psilocybe subcubensis Stropharia aeruginosa Stropharia coranilla Hohenbuehelia mastrucata Pleurotus cystidiosus Pleurotus eryngii Pleurotus florida Pleurotus eryngii var. eryngii Pleurotus eryngii var. ferulae Pleurotus ostreatus Pleurotus sajor-caju Pleurotus fockei Pleurotus pulmonarius Lactarius deliciosus Lactarius vellereus Lactarius indigo Russula delica Zjawiony 2004 Weber 1990 Rosa et al. 2003; Imtiaj & Lee 2007 Akyuz et al. 2010; Fagade & Oyelade 2009; Iwalokun et al. 2007; Surekha et al. 2011 Sterner et al. 1985; Ochoa-Zarzosa et al. 2011; Shittu 2006 Journal on New Biological Reports 2(2): 142-162 (2013) Table 1. contd..... Mycenaceae Mycena Mycena alcalina Xeromphalina Paxillaceae Favolaschia Filoboletus Paxillus Psathyrellaceae Psathyrella Panaeolus Coprinellus Pluteaceae Pluteus Volvariella Rhizopogonaceae Rhizopogon Suillaceae Suillus Lyophyllaceae Gomphidiaceae Lyophyllum Chroogomphus Hygrophoraceae Mycena aurantiomarginata Mycena leucogala Mycena maculata Xeromphalina junipericola Xeromphalina tenuipes Favolaschia sp. Filoboletus sp. Paxillus involutus Paxillus panuoides Rosa et al. 2003; Suay et al. 2000 Yamac & Bilgili 2006; Mustafa 2006 Ayodele & Idoko 2011 Psathyrella calcarea Psathyrella gracilis Psathyrella lacrymabunda Psathyrella sylvestris Psathyrella atroumbonata Panaeolus semiovatus Coprinellus micaceum Pluteus cubensis Ayodele & Idoko 2011; Surekha et Volvariella sp. Volvariella volvacea al. 2011 Rhizopogon luteolus Yamac & Bilgili Rhizopogon roseolus 2006, Mustafa 2006 Suillus luteus Suillus variegatus Suillus collitinus Lyophyllum decastes Chroogomphus rutilus Yamac & Bilgili 2006; Mustafa 2006 Pushpa 2010 Yamac & Bilgili 2006; Mustafa 2006 Hygrophorus Hygrophorus agathosmus Yamac & Bilgili 2006; Mustafa 2006 Phallaceae Dictyophora Imtiaj & Lee 2007 Auriculariaceae Auricularia Dictyophora indusiata Auricularia auricula Auricularia fuscosuccinea Auricularia polytricha 146 Fagade & Oyelade 2009 Rosa et al. 2003 Kiran R. Ranadive et al., 2013 Table 1. contd..... Meruliaceae Bjerkandera Cymatoderma Gloeoporus Hyphoderma Cerocorticium Irpex Heteroporus Phlebia Abortiporus Merulius Polyporaceae Cerrena Coriolopsis Coriolus Dichomitus Fomes Hexagonia Lentinus Lenzites Trametes 147 Bjerkandera adusta Cymatoderma dendriticum Gloeoporus thelephoroides Hyphoderma definitum Cerocorticium confluens Irpex destruens Irpex lacteus Heteroporus biennis Phlebia radiata Abortiporus biennis Merulius tremellosus Merulius corium Cerrena unicolor Coriolopsis byrsina Coriolopsis occidentalis Coriolopsis rigida Coriolopsis tricolor Coriolus consors Coriolus sanguineus Dichomitus squalens Fomes fomentarius Fomes juniperinus Fomes lignosus Hexagonia hydnoides Lentinus bertieri Lentinus crinitus Lentinus edodes Lentinus squarrosulus Lentinus striatulus Lentinus strigellus Lentinus strigosus var. strigosus Lentinus subnudus Lentinus villosus Lenzites elegans Lenzites thermophila Lenzites betulina Trametes cubensis Trametes pubescens Trametes versicolor Trametes villosa Trametes betulina Trametes gibbosa Trametes saepiara Trametes versicolor Florey et al. 1949 Mizuno 1995; Fowler 2000; Peintner 1998; Anchel et al. 1952, Fagade & Oyelade 2009; Yamac & Bilgili 2006; Mustafa 2006; Takeuchi et al. 1969; Ying et al. 1987; Kim et al 2001; Kavanagh et al. 1950: Imtiaz & Lee 2007; Ayodele & Idoko 2011 Journal on New Biological Reports 2(2): 142-162 (2013) Table 1. contd..... Panus Coriolus Daedaleopsis Perenniporia Polyporus Poria Pycnoporus Trichaptum Tyromyces Dendropolyporus Phanerochaetaceae Climacodon 148 Panus fulvus Coriolus versicolor Daedaleopsis confragosa Daedaleopsis flavida Daedaleopsis tricolor Perenniporia fraxinea Polyporus arcularius Polyporus benzoinus Polyporus betulinus Polyporus biformis Polyporus borealis Polyporus cinnabarinus Polyporus igniarius Polyporus meridionalis Polyporus ostriformis Polyporus palustris Polyporus rhizophilus Polyporus sulphureus Ployporus umbellatus Poria corticola Poria monticola Poria subacida Poria tenius Poria vaillantii Poria xantha Pycnoporus cinnabarinus Pycnoporus sanguineus Pycnoporus coccineus Trichaptum biforme Tyromyces duracinus Dendropolyporus pseudolacteus Dendropolyporus umbellatus Climacodon Rosa et al. 2003 pulcherrimus Kiran R. Ranadive et al., 2013 Table 1. contd..... Fomitopsidaceae Daedalea Fomitopsis Leptoporus Ischnoderma Laetiporus Fomitopsis Phaeolus Gloeophyllaceae Piptoporus Gloeophyllum Stereaceae Aleurodiscus Gloeocystidiellum Stereum Bankeraceae Hydnellum Sarcodon Meripilaceae Hydnopolyporus Meripilus Schizoporaceae Hyphodontia Hymenochaetaceae Inonotus Onnia Phellinus 149 Daedalea dickinsii Daedalea elegans Daedalea microzona Daedalea quercina Fomitopsis officinalis Leptoporus sp. Leptoporus mollis Ischnoderma benzoinum Laetiporus sulphureus Fomitopsis pinicola Fomitopsis officinalis Phaeolus schweinitzii Piptoporus betulinus Gloeophyllum odoratum Gloeophyllum sepiarium Aleurodiscus botryosus Aleurodiscus mirabilis Gloeocystidiellum porosum Stereum complicatum Stereum frustulosum Stereum hirsutum Stereum insignitum Stereum ostrea Hydnellum ferrugineum Sarcodon imbricatus, Hydnopolyporus fimbriatus Meripilus giganteus Hyphodontia subalutacea Inonotus hispidus Onnia tomentosa Phellinus sp. Phellinus adamantinus Phellinus aureobrunneus Phellinus badius Bose 1946; Bannur et al. 1967; Fagade & Oyelade 2009; Ofodile et al. 2010; Naranmandakh et al. 2008; Suay et al. 2000 Kahlos 1994 Imtiaj & Lee 2007 Yamac & Bilgili 2006; Mustafa 2006 Rosa et al. 2003 Kalyoncu et al. 2010 Suay et al. 2000 Balakumar et al. 2011; Florey et al. 1949; Cavill 1953, Bose & Chaudhury 1944; Lamrood 2004 Journal on New Biological Reports 2(2): 142-162 (2013) Table 1. contd..... Polystictus Ganodermataceae Ganoderma Auriscalpiaceae Lentinellus 150 Phellinus coffeatoporus Phellinus crocatus Phellinus fastuosus Phellinus gilvus Phellinus grenadensis Phellinus griseoporus Phellinus linteus Phellinus lividus Phellinus lloydii Phellinus merrillii Phellinus minutiporus Phellinus rimosus Phellinus sublinteus Phellinus swieteniae Polystictus sanguineus Ganoderma apense Ganoderma applanatum Ganoderma chalceum Ganoderma lipsiense Ganoderma lucidum Ganoderma lucidum var. lucidum Ganoderma multicornum Ganoderma multiplicatum Ganoderma oregonense Ganoderma perzonatum Ganoderma pfeifferi Ganoderma pfeifferi var. borneense Ganoderma poonensis Ganoderma praelongum Ganoderma resinaceum Ganoderma stipitatum Ganoderma carnosum Lentinellus omphalodes Smania 2001; Bhosale et al. 2010; Yoon et al. 1994; Wasser & Weis 1997a; Coletto et al 1981; Sheena et al. 2003; Fagade & Oyelade 2009; Quereshi et al. 2010; Bhosale et al. 2010; Mothana et al. 2000; Wilsely 2008; Yamac & Bilgili 2006 Běhal 2003 Kiran R. Ranadive et al., 2013 Table 1. contd..... Ascomycetes (Lichenised) Peniophoraceae Peniophora Gomphaceae Schizophyllaceae Ramaria Schizophyllum Sparassidaceae Sparassis Sparassis crispa Clavaridelphaceae Clavaridelphus Clavaridelphus truncatus Hydnaceae Hydnum Hydnum repandum, Yamac & Bilgili 2006; Mustafa 2006 Dacrymycetaceae Arthoniaceae Calocera Arthothelium Suay et al. 2000 Behera et al. 2007 Physciaceae Heterodermia Umbilicariaceae Lasallia Umbilicaria Parmeliaceae Parmelia Parmotrema Calocera viscosa Arthothelium awasthii Heterodermia podocarpa Lasallia pustulata Umbilicaria crustulosa Umbilicaria cylindrica Parmelia sulcata Parmotrema tinctorium Parmeliopsis hyperopta Usnea ghattensis Lecanora frustulosa, Parmeliopsis Ascomycetes (NonLichenised) Lecanoraceae Usnea Lecanora Ramalinaceae Cordycipitaceae Morchellaceae Ramalina Cordyceps Morchella Xylariaceae Daldinia Chaetomiaceae Chaetomium 151 Peniophora cinerea Peniophora incarnata Peniophora quercina Peniophora utriculosa Ramaria flava Schizophyllum commune Rosa et al. 2003 Gezer et al. 2006 Chang et al. 1978; Fagade & Oyelade 2009. Lindequist et al. 2005 Yamac & Bilgili 2006; Mustafa 2006 Behera et al. 2007 Rankovic 2007 et al. Rankovic et al. 2007; Branislav et al. 2010; Behera et al. 2007; Dulger et al.1998, 1997 Branislav et al. 2010 Ramalina farinacea Turgay et al. 2004 Cordyceps sobolifera Imtiaj & Lee 2007 Morchella conica Torkoglu et al. 2006 Daldinia concentrica Gbolagade & Fasidi 2005 Chaetomium Srimathi et al. 2011 atrobrunneum Chaetomium globossum Chaetomium funicola Chaetomium strumarium Journal on New Biological Reports 2(2): 142-162 (2013) Table 1. contd..... Pezizaceae Nectriaceae Diaporthaceae Diaporthe Terfezia boudieri Tirmania sp. Sordariomycetes Fusarium solani Fusarium graminearum Diaporthe sp. Pleosporaceae Alternaria Alternaria sp. Ding 2010 Glomerellaceae Amphishaeriaceae Botryosphaeriaceae Trichocomaceae Colletotrichum Pestalotiopsis Guignardia Penicillum Colletotrichum sp. Pestalotiopsis sp. Guignardia vaccinii Penicillum sp. Penicillium expansum Aspergillus niger Aspergillus flavus Rickenella fibula Zythia sp. Nigrospora sp. Ding 2010 Ding 2010 Ding 2010 Ding 2010; Praveena & Palem 2011 Aspergillus Incertae sedis Akyuz et al. 2010; Ding T. 2010 Terfezia Tirmania Sordariomycetes Fusarium Incertae sedis Rickenella Zythia Nigrospora Tayung et al. 2011; Praveena & Palem 2011 Ding 2010 Ding 2010 Table 2. Total count of families, genera and species showing antimicrobial properties Fungal Group Total Families Total Genera Total Species Basidiomycetes 45 122 281 Ascomycetes (Lichenised) 06 10 11 Ascomycetes (Non-Lichenised) 12 15 21 Incertae sedis 01 03 03 Total 64 150 316 152 Kiran R. Ranadive et al., 2013 Fig 1. Graphical representation of total count of Families, Genera and Species showing Antimicrobial Properties Fig 2. Number of Species from different families showing antimicrobial activity 153 Journal on New Biological Reports 2(2): 142-162 (2013) Table 3. Species wise dominant families showing antimicrobial properties Number of species showing Family antimicrobial activity Polyporaceae 64 Agaricaceae 22 Hymenochaetaceae 21 Tricholomataceae 16 Fomitopsidaceae 13 Meruliaceae 12 Physalacriaceae, Pleurotaceae and Marasmiaceae 10 Stereaceae and Mycenaceae 08 Amanitaceae, Auriculariaceae, Incertae sedis, Pezizaceae, Pluteaceae, 03 Suillaceae and Umbilicariaceae Bankeraceae, Gloeophyllaceae, Inocybaceae, Meripilaceae, Nectriaceae, 02 Paxillaceae and Rhizopogonaceae Amphishaeriaceae, Arthoniaceae, Clavaridelphaceae, Auriscalpiaceae, Coniophoraceae, Botryosphaeriaceae, Cordycipitaceae, Cyphellaceae, Dacrymycetaceae, Diaporthaceae, Entolomataceae, Fistulinaceae, Glomerellaceae, Gomphaceae, Gomphidiaceae , Hydnaceae, Hygrophoraceae, Lecanoraceae, Lyophyllaceae , Morchellaceae, Niaceae, Phallaceae, 01 Phanerochaetaceae, Physciaceae, Pleosporaceae, Ramalinaceae, Schizophyllaceae, Schizoporaceae, Sparassidaceae and Xylariaceae Total: 64 Families 316 *Total 03 Unknown families quoted under Incertae sedis Table 4. List of families of bacteria used to check the antimicrobial activity Name of the Family Aeromonadaceae Bacillaceae Brucellaceae Corynebacteriaceae Species Aeromonas hydrophelia Bacillus cereus, B.megaterium,B. mycoides, B. pumilllus,B. subtilis, Brucella abortus Cornyebacterium xerosis Name of the Family Aeromonadaceae Bacillaceae Total Species of the Families 01 05 Brucellaceae Corynebacteriaceae 01 01 154 Kiran R. Ranadive et al., 2013 Table 4 contd..... Enterobacteriaceae E. coli, Enterobacter aerogenes, E. cloacae, Enterococcus faecalis, Klebsiella pneumonia, Salmonella enteric, S. typhi, S. typhimurium, S. typhisuis, Shigella flexneri, Yersinia enterocolis, Flavobacteriaceae Flavobacterium sp. Helicobacteraceae Helicobacter pylori Listeriaceae Listeria monocytogenes Micrococcaceae Micrococcus luteus Pseudomonadaceae Pseudomonas aeruginosa, Pseudomonas syringa Staphylococcaceae Staphyllcoccus aureus, S. epidermis, S. faecalis, S. sp. Streptococcaceae Streptococcus mutans Streptomycetaceae Streptomyces pyrogens Fig 3. Generic dominance of the Bacterial Families 155 Enterobacteriaceae 12 Flavobacteriaceae Helicobacteraceae Listeriaceae Micrococcaceae Pseudomonadaceae Staphylococcaceae 01 01 01 01 02 04 Streptococcaceae Streptomycetaceae 01 01 Journal on New Biological Reports 2(2): 142-162 (2013) Table 5. List of fungi used for checking antimicrobial activity Family Ceratobasidiaceae Trichocomaceae Genus Rhizoctonia Aspergillus Mucoraceae Mucor Saccharomycetaceae Scaccharomyces Hypocreaceae Trichoderma Arthrodermataceae Trichophyton Species Rhizoctonia solani Aspergillus flavus Aspergillus fumigates Aspergillus niger Paecilomyces variotii Penicillium notatum Penicillium purpurescens Penicillium sp. Penicillium verrucosum Botrytis cinerea, Cladosporium herbarium Epidermophyton spp. Fusarium oxysporum Fusarium oxysporum f. sp. vasinfectum Mucor indicus Mucor mucedo Scaccharomyces cerevisiae Trichoderma harsianum Trichophyton sp. Pleosporaceae Curvularia Alternaria Candida Curvularia sp. Alternaria sp. Candida albicans Paecilomyces Penicillium Sclerotiniaceae Davidiellaceae Botrytis Cladosporium Arthrodermataceae Epidermophyton Nectriaceae Fusarium Incertae sedis Candida glabrata Candida tropicalis 156 Reference Ding et al. 2010 Balakumar et al. 2011 Balakumar et al. 2011 Pushpa & Purushottama 2010 Pushpa & Purushottama 2010 Fagade and Oyelade, 2009, Nyyetabura et al. 2010, Srimathi et al. 2011, Akyuz et al. 2010, Bhosale et al. 2010, Rankovic et al. 2010, Pushpa & Purushottama 2010, Yamac & Bilgili 2006 Akyuz et al. 2010 Naranmandakh et al. 2010 Nyyetabura et al. 2010 Rankovic et al. 2010 Turgay T.et al. 2004 Rankovic et al. 2010 Balakumar et al. 2011 Rankovic et al. 2010 Imtiaj and Lee 2007, Rankovic et al. 2010 Ofodile et al. 2010 Akyuz et al. 2010 Ding et al. 2010 Ding et al. 2010 Balakumar et al. 2011 Rankovic et al. 2010 Yamac & Bilgili 2006 Rankovic et al. 2010 Akyuz et al. 2010 Kiran R. 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