Phytochemistry Reviews

, Volume 14, Issue 6, pp 975–991 | Cite as

Preliminary evidences of the direct and indirect antimicrobial activity of 12 plants used in traditional medicine in Africa

  • Lucy Catteau
  • Françoise Van Bambeke
  • Joëlle Quetin-Leclercq
Article

Abstract

In a world of increasing resistance to current antibiotics, search of novel therapeutic options is urgently needed. The aim of this work was to screen plant crude extracts for direct or indirect (inhibition of resistance) antimicrobial activity. Four crude extracts from 12 plants traditionally used in Africa for the treatment of infections were obtained by successive extraction with hexane, dichloromethane, ethyl acetate, and methanol. All extracts were tested against Staphylococcus aureus MRSA ATCC33591 [resistant to β-lactams by production of β-lactamases and of a modified PBP target (PBP2a)]. Direct antimicrobial activity was tested by determination of Minimal Inhibitory Concentrations (MIC), and indirect activity, by determining interactions between antibiotics and extracts using checkerboard titration and calculation of Fractional Inhibitory Concentration Index (FICI; synergy: FICI ≤ 0.5; additivity: FICI ≤ 1). Combined antibiotics were ampicillin (sensitive to resistance mediated by β-lactamases and PBP2a) and oxacillin (sensitive to resistance mediated by PBP2a only). The dichloromethane extract of Vitellaria paradoxa leaves, the methanol extracts of Vitellaria paradoxa, Cola gigantea leaves and twigs, and of Tapinanthus bangwensis aerial parts showed direct antimicrobial activity (MIC 250–500 mg/L). The methanol extracts of Vitellaria paradoxa and Cola gigantea leaves and twigs showed additive or synergistic effects with oxacillin and ampicillin on MRSA ATCC33591 (FICI 0.28–1), suggesting a possible inhibition of PBP2a. The methanol extract of Tapinanthus bangwensis aerial parts and Anchomanes difformis roots improved the activity of ampicillin only (FICI 0.38–1), suggesting β-lactamase inhibition. Polyphenols and particularly tannins were shown to be responsible for these last effects, at least partially for Vitellaria paradoxa. These data need further research aiming at identifying the active compounds in these extracts.

Keywords

Plant extracts Resistance modifying agent MRSA β-Lactams Tannins 

Notes

Acknowledgments

The authors are grateful to Mr. Agabani (botanist of University of Abomey-Calavi, Cotonou, Benin) for plant collections and to Maude Bourlet for her skillful technical assistance. F.V.B. is Maître de Recherches of the Belgian Fonds de la Recherche Scientifique. The authors gratefully thank the Belgian Fonds de la Recherche Scientifique for financial support.

References

  1. Abah SE, Egwari L, Mosaku TO (2011) In vitro antimicrobial screening on Anchomanes difformis (Blume) Engl. leaves and rhizomes against selected pathogens of public health importance. Adv Biol Res 5:221–225Google Scholar
  2. Abreu AC, McBain AJ, Simões M (2012) Plants as sources of new antimicrobials and resistance-modifying agents. Nat Prod Rep 29:1007–1021. doi: 10.1039/C2NP20035J PubMedCrossRefGoogle Scholar
  3. Adeleke O, Adetunji T (2010) Antimicrobial activity of Anchomanes difformis (Blume) Engl. [family ARACEAE]. J Life Phys Sci 2:87–90Google Scholar
  4. Adjanohoun EJ, Adjakidje V, Ahyi MR, Aké assi L, Akoegninou A, d’Almeida J, Apovo F, Boukef K, Chadare M, Cusset G, Dramane K, Eyme J, Gassita JN, Gbaguidi N, Goudote E, Guinko P, Houngnon P, Lo I, Keita A, Kiiniffo HV, Kone-Bamba D, Musampa Nseyya A, Saadou M, Sodogandji T, de Souza S, Tchabi A, Zinsou T (1989) Contribution aux études ethnobotaniques et floristiques en République Populaire du Bénin. In: Médecine Traditionnelle et Pharmacopée. CotonouGoogle Scholar
  5. Agbo MO, Lai D, Okoye FBC, Osadebe PO, Proksch P (2013) Antioxidative polyphenols from Nigerian mistletoe Loranthus micranthus (Linn.) parasitizing on Hevea brasiliensis. Fitoterapia 86:78–83. doi: 10.1016/j.fitote.2013.02.006 PubMedCrossRefGoogle Scholar
  6. Agyare C, Koffuor GA, Boamah VE, Adu F, Mensah KB, Adu-Amoah L (2012) Antimicrobial and anti-inflammatory activities of Pterygota macrocarpa and Cola gigantea (Sterculiaceae). Evid Based Complement Altern Med 2012:e902394. doi: 10.1155/2012/902394 CrossRefGoogle Scholar
  7. Ahua KM, Ioset J-R, Diallo D, Mauël J, Hostettmann K (2007) Antileishmanial activities associated with plants used in the Malian traditional medicine. J Ethnopharmacol 110:99–104PubMedCrossRefGoogle Scholar
  8. Aliyu AB, Musa AM, Oshanimi JA, Ibrahim HA, Oyewale AO (2008) Phytochemical analyses and mineral elements composition of some medicinal plants of Northern Nigeria. Niger J Pharm Sci 7:119–125Google Scholar
  9. Aniszewski T (2007) Alkaloids: secrets of life: aklaloid chemistry, biological significance, applications and ecological role. Elsevier, AmsterdamGoogle Scholar
  10. Asase A, Kokubun T, Grayer RJ, Kite G, Simmonds MSJ, Oteng-Yeboah AA, Odamtten GT (2008) Chemical constituents and antimicrobial activity of medicinal plants from Ghana: Cassia sieberiana, Haematostaphis barteri, Mitragyna inermis and Pseudocedrela kotschyi. Phytother Res 22:1013–1016. doi: 10.1002/ptr.2392 PubMedCrossRefGoogle Scholar
  11. Ayankunle AA, Kolawole OT, Adesokan AA, Akiibinu MO (2012) Antibacterial activity and sub-chronic toxicity studies of vitellaria paradoxa stem bark extract. J Pharmacol Toxicol 7:298–304. doi: 10.3923/jpt.2012.298.304 CrossRefGoogle Scholar
  12. Badmus JA, Odunola OA, Obuotor EM, Oyedapo OO (2009) Phytochemicals and in vitro antioxidant potentials of defatted methanolic extract of Holarrhena floribunda leaves. Afr J Biotechnol 9:340–346Google Scholar
  13. Balogun SO, Oladosu IA, Liu Z (2014) Chemical compositions and antioxidant potential of essential oils from leaves and flowers of Allophylus africanus. J Essent Oil Bear Plants 17:769–775. doi: 10.1080/0972060X.2014.895176 CrossRefGoogle Scholar
  14. Barber M, Waterworth PM (1964) Penicillinase-resistant Penicillins. Br Med J 2:344–349PubMedCentralPubMedCrossRefGoogle Scholar
  15. Bero J, Ganfon H, Jonville M-C, Frédérich M, Gbaguidi F, DeMol P, Moudachirou M, Quetin-Leclercq J (2009) In vitro antiplasmodial activity of plants used in Benin in traditional medicine to treat malaria. J Ethnopharmacol 122:439–444. doi: 10.1016/j.jep.2009.02.004 PubMedCrossRefGoogle Scholar
  16. Bogne KP, Penlap BV, Lontsi D, Etoa F-X (2007) Antibacterial activities of the extracts and conessine from Holarrhena floribunda G. Don. (Apocynaceae). Afr J Tradit Complement Altern Med 4:352–356PubMedGoogle Scholar
  17. Bonapace CR, Bosso JA, Friedrich LV, White RL (2002) Comparison of methods of interpretation of checkerboard synergy testing. Diagn Microbiol Infect Dis 44:363–366. doi: 10.1016/S0732-8893(02)00473-X PubMedCrossRefGoogle Scholar
  18. Bruneton J (2009) Pharmacognosie, phytochimie, plantes médicinales (4e ed.), Tec & Doc ed Lavoisier, ParisGoogle Scholar
  19. Buyck JM, Tulkens PM, Van Bambeke F (2015) Activities of antibiotic combinations against resistant strains of Pseudomonas aeruginosa in a model of infected THP-1 monocytes. Antimicrob Agents Chemother 59:258–268. doi: 10.1128/AAC.04011-14 PubMedCentralPubMedCrossRefGoogle Scholar
  20. Cha J-D, Moon S-E, Kim J-Y, Jung E-K, Lee Y-S (2009) Antibacterial activity of sophoraflavanone G isolated from the roots of Sophora flavescens against methicillin-resistant Staphylococcus aureus. Phytother Res 23:1326–1331. doi: 10.1002/ptr.2540 PubMedCrossRefGoogle Scholar
  21. Chanda S, Rakholiya K (2011) Indian combination therapy: synergism between natural plant extracts and antibiotics against infectious diseases. In: Mendez-Vilas A (ed) Science against microbial pathogens: communicating current research and technological advances. Formatex Research Center, Spain, pp 520–529Google Scholar
  22. Chen H-Y, Ye X-L, Cui X-L, He K, Jin Y-N, Chen Z, Li X-G (2012) Cytotoxicity and antihyperglycemic effect of minor constituents from rhizoma coptis in HepG2 cells. Fitoterapia 83:67–73. doi: 10.1016/j.fitote.2011.09.014 PubMedCrossRefGoogle Scholar
  23. Chinworrungsee M, Wiyakrutta S, Sriubolmas N, Chuailua P, Suksamrarn A (2008) Cytotoxic activities of trichothecenes isolated from an endophytic fungus belonging to order Hypocreales. Arch Pharm Res 31:611–616. doi: 10.1007/s12272-001-1201-x PubMedCrossRefGoogle Scholar
  24. Chung K-T, Stevens SE Jr, Lin W-F, Wei CI (1993) Growth inhibition of selected food-borne bacteria by tannic acid, propyl gallate and related compounds. Lett Appl Microbiol 17:29–32. doi: 10.1111/j.1472-765X.1993.tb01428.x CrossRefGoogle Scholar
  25. Coates A, Hu Y, Bax R, Page C (2002) The future challenges facing the development of new antimicrobial drugs. Nat Rev Drug Discov 1:895–910. doi: 10.1038/nrd940 PubMedCrossRefGoogle Scholar
  26. Comini LR, Núñez Montoya SC, Páez PL, Argüello GA, Albesa I, Cabrera JL (2011) Antibacterial activity of anthraquinone derivatives from Heterophyllaea pustulata (Rubiaceae). J Photochem Photobiol, B 102:108–114. doi: 10.1016/j.jphotobiol.2010.09.009 CrossRefGoogle Scholar
  27. Cowan MM (1999) Plant Products as Antimicrobial Agents. Clin Microbiol Rev 12:564–582PubMedCentralPubMedGoogle Scholar
  28. Cushnie TPT, Lamb AJ (2005) Antimicrobial activity of flavonoids. Int J Antimicrob Agents 26:343–356. doi: 10.1016/j.ijantimicag.2005.09.002 PubMedCrossRefGoogle Scholar
  29. Dilika F, Bremner PD, Meyer JJM (2000) Antibacterial activity of linoleic and oleic acids isolated from Helichrysum pedunculatum: a plant used during circumcision rites. Fitoterapia 71:450–452. doi: 10.1016/S0367-326X(00)00150-7 PubMedCrossRefGoogle Scholar
  30. Doyinsola Idowu, Adedayo Adebiyi, Olutayo Olajide, Michael Afolayan, Abayomi Orishadipe, Moses Omojola, Thomas Sunday (2012) Phytochemical, antioxidant and cytotoxicity properties of Anchomanes difformis (Bl.) Engl. tuber extract. Int J Appl Chem 8:173–181Google Scholar
  31. Drawz SM, Bonomo RA (2010) Three decades of beta-lactamase inhibitors. Clin Microbiol Rev 23:160–201. doi: 10.1128/CMR.00037-09 PubMedCentralPubMedCrossRefGoogle Scholar
  32. Dua VK, Verma G, Singh B, Rajan A, Bagai U, Agarwal DD, Gupta NC, Kumar S, Rastogi A (2013) Anti-malarial property of steroidal alkaloid conessine isolated from the bark of Holarrhena antidysenterica. Malar. J. 12:194. doi: 10.1186/1475-2875-12-194 PubMedCentralPubMedCrossRefGoogle Scholar
  33. Efuntoye MO, Ayodele AE, Thomas BT, Ajayi TO (2010) Does host plant affect the antibacterial activity of Tapinanthus bangwensis (Engl. and K. Krause) Danser (Loranthaceae). J Med Plants Res 4:1281–1284Google Scholar
  34. Ekhaise FO, Ofoezie VG, Enobakhare DA (2010) Antibacterial properties and preliminary phytochemical analysis of methanolic extract of mistletoe (Tapinanthus bangwensis). Bayero J Pure Appl Sci 3:65–68. doi: 10.4314/bajopas.v3i2.63223 Google Scholar
  35. Eliopoulos G, Moellering RC (1996) Antimicrobial combinations. Antibiotics in laboratory medicine. Lorian V, Baltimore, pp 330–396Google Scholar
  36. El-Mahmood AM, Doughari JH, Ladan N (2008) Antimicrobial screening of stem bark extracts of Vitellaria paradoxa against some enteric pathogenic microorganisms. Afr J Pharm Pharmacol 2:089–094Google Scholar
  37. EUCAST (2000) Terminology relating to methods for the determination of susceptibility of bacteria to antimicrobial agents. Clin Microbiol Infect 6:503–508. doi: 10.1046/j.1469-0691.2000.00149.x CrossRefGoogle Scholar
  38. Fotie J, Bohle DS, Leimanis ML, Georges E, Rukunga G, Nkengfack AE (2006) Lupeol long-chain fatty acid esters with antimalarial activity from Holarrhena floribunda. J Nat Prod 69:62–67. doi: 10.1021/np050315y PubMedCrossRefGoogle Scholar
  39. Fu J, Cheng K, Zhang Z, Fang R, Zhu H (2010) Synthesis, structure and structure–activity relationship analysis of caffeic acid amides as potential antimicrobials. Eur J Med Chem 45:2638–2643. doi: 10.1016/j.ejmech.2010.01.066 PubMedCrossRefGoogle Scholar
  40. Garba S, Salihu L (2011) Antibacterial activities of 2-O-butyl-1-O-(2′-ethylhexyl) benzene-1,8-dicarboxylate and 1-phenyl-1,4-pentanedione isolated from Vitellaria paradoxa root bark. Asian J Sci Res 4:149–157. doi: 10.3923/ajsr.2011.149.157 CrossRefGoogle Scholar
  41. Gershenzon J (1984) Changes in the levels of plant secondary metabolites under water and nutrient stress. In: Timmermann BN, Steelink C, Loewus FA (eds) Phytochemical adaptations to stress, recent advances in phytochemistry. Springer, New York, pp 273–320CrossRefGoogle Scholar
  42. Gibbons S (2004) Anti-staphylococcal plant natural products. Nat Prod Rep 21:263–277. doi: 10.1039/B212695H PubMedCrossRefGoogle Scholar
  43. Gibbons S (2005) Plants as a source of bacterial resistance modulators and anti-infective agents. Phytochem Rev 4:63–78. doi: 10.1007/s11101-005-2494-9 CrossRefGoogle Scholar
  44. Hadler JL, Petit S, Mandour M, Cartter M (2012) Trends in Invasive Infection with Methicillin-Resistant Staphylococcus aureus, Connecticut, USA, 2001–2010. Emerg. Infect. Dis. J. 18:917–924CrossRefGoogle Scholar
  45. Hall JB, Aebischer DP, Tomlinson HF, Osei-Amaning E, Hindle JR (1996) Vitellaria paradoxa: a monograph. School of Agricultural and Forest Sciences, University of WalesGoogle Scholar
  46. Hemaiswarya S, Kruthiventi AK, Doble M (2008) Synergism between natural products and antibiotics against infectious diseases. Phytomedicine 15:639–652. doi: 10.1016/j.phymed.2008.06.008 PubMedCrossRefGoogle Scholar
  47. Houghton PJ, Raman A (1998) Laboratory handbook for the fractionation of natural extracts. Chapman and Hall, LondonCrossRefGoogle Scholar
  48. Janot MM, Cave A, Goutarel R (1960) Steroid alkaloids. Holaphyllamine and holamine, alkaloids from Holarrhena floribunda (G. Don) Dur. and Schinz. Comptes Rendus Hebd. Séances Académie Sci. 251:559–561Google Scholar
  49. Jiofack T, Fokunang C, Guedje N, Kemeuze V, Fongnzossie E, Nkongmeneck BA, Mapongmetsem PM, Tsabang N (2010) Ethnobotanical uses of medicinal plants of two ethnoecological regions of Cameroon. Int J Med Med Sci 2:60–79Google Scholar
  50. Johnson AP (2011) Methicillin-resistant Staphylococcus aureus: the European landscape. J Antimicrob Chemother 66:43–48. doi: 10.1093/jac/dkr076 Google Scholar
  51. Kalant H (1965) The pharmacology of semisynthetic antibiotics. Can Med Assoc J 93:839–843PubMedCentralPubMedGoogle Scholar
  52. Kamagaju L (2014) Problem of skin depigmentation in Rwanda. Modulators of tyrosinase extracted from plants used in traditional medicine. Thesis in Biomedical and Pharmaceutical Sciences, ULB, BrusselsGoogle Scholar
  53. Karou D, Savadogo A, Canini A, Yameogo S, Montesano C, Simpore J, Colizzi V, Traore AS (2005) Antibacterial activity of alkaloids from Sida acuta. Afr J Biotechnol. doi: 10.4314/ajb.v4i12.71463 Google Scholar
  54. Kim HS, Han SS, Oh KW, Jeong TS, Nam KY (1987) Effects of Ginseng saponin on the antimicrobial activities of some antibiotics. Korean J Mycol 15:87–91Google Scholar
  55. Kuete V (2010) Potential of Cameroonian plants and derived products against microbial infections: a review. Planta Med 76:1479–1491. doi: 10.1055/s-0030-1250027 PubMedCrossRefGoogle Scholar
  56. Lagnika L, Weniger B, Attioua B, Jensen O, Anthaume C, Sanni A, Kaiser M, Lobstein A, Vonthron-Senecheau C (2012) Trypanocidal activity of diarylheptanoids from Schrankia leptocarpa DC. South Afr J Bot 83:92–97. doi: 10.1016/j.sajb.2012.06.011 CrossRefGoogle Scholar
  57. Latifou Lagnika UP (2012) Chemical analysis, antimicrobial and antioxidant activities of eight extracts from Schrankia leptocarpa L. Afr J Biotechnol 11:13739–13745. doi: 10.5897/AJB12.633 Google Scholar
  58. Leboeuf M, Cavé A, Goutarel R (1969) Steroid alkaloids. LXXXII. (16). Chemical composition of the leaves of Holarrhena floribunda Dur. et Schinz. Isolation of progesterone and 4 new alkaloids: methylholaphylline, holaphyllinol, holaphyllidine and dihydroholaphyllamine. Ann Pharm Fr 27:217–228PubMedGoogle Scholar
  59. Lee Y-S, Kang O-H, Choi J-G, Oh Y-C, Keum J-H, Kim S-B, Jeong G-S, Kim Y-C, Shin D-W, Kwon D-Y (2010) Synergistic effect of emodin in combination with ampicillin or oxacillin against methicillin-resistant Staphylococcus aureus. Pharm Biol 48:1285–1290. doi: 10.3109/13880201003770150 PubMedCrossRefGoogle Scholar
  60. Loukaci A, Kayser O, Bindseil K, Siems K, Frevert J, Abreu PM (2000) New trichothecenes isolated from Holarrhena floribunda. J Nat Prod 63:52–56PubMedCrossRefGoogle Scholar
  61. Lowy FD (1998) Staphylococcus aureus infections. N Engl J Med 339:520–532. doi: 10.1056/NEJM199808203390806 PubMedCrossRefGoogle Scholar
  62. Manríquez-Torres J, Zúñiga-Estrada A, González-Ledesma M, Torres-Valencia JM (2007) The antibacterial metabolites and proacacipetalin from Acacia cochliacantha. J Mex Chem Soc 51:228–231Google Scholar
  63. Mathabe MC, Hussein AA, Nikolova RV, Basson AE, Meyer JJM, Lall N (2008) Antibacterial activities and cytotoxicity of terpenoids isolated from Spirostachys africana. J Ethnopharmacol 116:194–197. doi: 10.1016/j.jep.2007.11.017 PubMedCrossRefGoogle Scholar
  64. Mbouangouere RN, Tane P, Ngamga D, Khan SN, Choudhary MI, Ngadjui BT (2007) A new steroid and α-glucosidase inhibitors from Anthocleista schweinfurthii. Res J Med Plant 1:106–111CrossRefGoogle Scholar
  65. Mezui C, Longo F, Nkenfou C, Sando Z, Ndeme E, Vernyuy Tan P (2015) Evalutation of acute and subacute tovicity of stem bark aqueous extract of Anthocleista schweinfurthii (Loganiaceae). World J Pharm Pharm Sci 4:197–208Google Scholar
  66. Miller RR, Price JR, Batty EM, Didelot X, Wyllie D, Golubchik T, Crook DW, Paul J, Peto TEA, Wilson DJ, Cule M, Ip CLC, Day NPJ, Moore CE, Bowden R, Llewelyn MJ (2014) Healthcare-associated outbreak of meticillin-resistant Staphylococcus aureus bacteraemia: role of a cryptic variant of an epidemic clone. J Hosp Infect 86:83–89. doi: 10.1016/j.jhin.2013.11.007 PubMedCentralPubMedCrossRefGoogle Scholar
  67. Moriarity DM, Huang J, Yancey CA, Zhang P, Setzer WN, Lawton RO, Bates RB, Caldera S (1998) Lupeol is the cytotoxic principle in the leaf extract of Dendropanax cf. querceti. Planta Med 64:370–372PubMedCrossRefGoogle Scholar
  68. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55–63PubMedCrossRefGoogle Scholar
  69. Ndukwe IG, Amupitan JO, Isah Y, Adegoke KS (2007) Phytochemical and antimicrobial screening of the crude extracts from the root, stem bark and leaves of Vitellaria paradoxa (Gaertn. F). Afr J Biotechnol 6:1905–1909Google Scholar
  70. Ngbolua KN, Mubindoukila Rosie Esther N, Mpiana Pius T, Ashande Masengo C, Robijaona Baholy, Ruphin Fatiany Pierre, Takoy L, Ekutsu Grégoire E, Gbolo Zoawe B (2014) In vitro assessment of antibacterial and antioxidant activities of a congolese medicinal plant species Anthocleista schweinfurthii Gilg (Gentianaceae). J Mod Drug Discov Drug Deliv Res 3:1–6. doi: 10.15297/JMDDR.V1I3.03 Google Scholar
  71. Njayou FN, Moundipa PF, Tchana AN, Ngadjui BT, Tchouanguep FM (2008) Inhibition of microsomal lipid peroxidation and protein oxidation by extracts from plants used in Bamun folk medicine (Cameroon) against hepatitis. Afr J Tradit Complement Altern Med 5:278–289PubMedCentralPubMedGoogle Scholar
  72. Nondo RSO, Mbwambo ZH, Kidukuli AW, Innocent EM, Mihale MJ, Erasto P, Moshi MJ (2011) Larvicidal, antimicrobial and brine shrimp activities of extracts from Cissampelos mucronata and Tephrosia villosa from coast region, Tanzania. BMC Complement Altern Med 11:33. doi: 10.1186/1472-6882-11-33 PubMedCrossRefGoogle Scholar
  73. Nwodo NJ, Brun R, Osadebe PO (2007) In vitro and in vivo evaluation of the antitrypanosomal activity of fractions of Holarrhena africana. J Ethnopharmacol 113:556–559. doi: 10.1016/j.jep.2007.07.018 PubMedCrossRefGoogle Scholar
  74. Odiba JO, Musa AM, Hassan HS, Yahaya SM, Okolo EI (2014) Antimicrobial activity of isolated Stigmast-5-en-3β-ol (β-sitosterol) from honeybee propolis from North-Western, Nigeria. Int J Pharma Sci Res 5:908–918Google Scholar
  75. Ogechukwu OE, Ogoamaka OP, Sylvester NC, Hassan A, Debbab A, Okechukwu EC, Kawamura A, Peter P (2011) Steroids and triterpenoids from Eastern Nigeria mistletoe, Loranthus micranthus Linn. (Loranthaceae) parasitic on Kola acuminata with immunomodulatory potentials. Phytochem Lett 4:357–362. doi: 10.1016/j.phytol.2011.07.011 Google Scholar
  76. Ogechukwu OE, Ogoamaka OP, Kawamura A, Hassan A, Debbab A et al (2012) Three-(−) catechin-O-rhamnosides from the Eastern Nigeria Mistletoe with potent immunostimulatory and antioxidant activities. Biomolecul 1:2CrossRefGoogle Scholar
  77. Ogunwande IA, Bello MO, Olawore ON, Muili KA (2001) Phytochemical and antimicrobial studies on Butyrospermum paradoxum. Fitoterapia 72:54–56. doi: 10.1016/S0367-326X(00)00238-0 PubMedCrossRefGoogle Scholar
  78. Oladosu IA, Balogun SO, Ademowo GO (2013) Phytochemical screening, antimalarial and histopathological studies of Allophylus africanus and Tragia benthamii. Chin. J. Nat. Med. 11:371–376. doi: 10.1016/S1875-5364(13)60054-0 PubMedCrossRefGoogle Scholar
  79. Oladosu IA, Balogun SO, Liu Z-Q (2015) Chemical constituents of Allophylus africanus. Chin. J. Nat. Med. 13:133–141. doi: 10.1016/S1875-5364(15)60017-6 PubMedGoogle Scholar
  80. Olutayo Olajide, Michael Afolayan, John Adewusi Adepoju, Olusola Adeyanju (2012) Antimicrobial activity and Elemental analysis of Cassia siberiana leaves Using Atomic Absorption Spectrometer. J. Nat. Prod. Plant Resour. 2:9–18Google Scholar
  81. Omeje EO, Osadebe PO, Nworu CS, Nwodo JN, Obonga WO, Kawamura A, Esimone CO, Proksch P (2011) A novel sesquiterpene acid and an alkaloid from leaves of the Eastern Nigeria mistletoe, Loranthus micranthus with potent immunostimulatory activity on C57BL6 mice splenocytes and CD69 molecule. Pharm Biol 49:1271–1276. doi: 10.3109/13880209.2011.621129 PubMedCrossRefGoogle Scholar
  82. Onyema CT, Ajiwe VIE (2014a) Phytochemical and anti-microbial analysis of the leaves of Cola gigantea (Sterculiaceae). Int J Appl Sci Technol 4:119–126Google Scholar
  83. Onyema CT, Ajiwe VIE (2014b) Phytochemical and antimicrobial analysis of the stems of Cola gigantea (Sterculiacea). Int J Eng Sci 3:01–11Google Scholar
  84. Otsuka N, Liu M-H, Shiota S, Ogawa W, Kuroda T, Hatano T, Tsuchiya T (2008) Anti-methicillin resistant Staphylococcus aureus (MRSA) compounds isolated from Laurus nobilis. Biol Pharm Bull 31:1794–1797PubMedCrossRefGoogle Scholar
  85. Oyetayo VO (2007) Comparative studies of the phytochemical and antimicrobial properties of the leaf, stem and tuber of Anchomanes difformis. J Pharmacol Toxicol 2:407–410. doi: 10.3923/jpt.2007.407.410 CrossRefGoogle Scholar
  86. Paris R, Etchepare S (1967) On the polyphenols of Cassia sieberiana DC. Isolation of l-epicatechol and leucopelargonidol. Ann Pharm Fr 25:343–346PubMedGoogle Scholar
  87. Paris RR, Foucaud A (1959) Flavonoids in the leaves of Holarrhena floribunda G. Don (Durand and Schinz): isolation of a flavonoside identified as isoquercitroside. Comptes Rendus Hebd Séances Académie Sci 248:2634–2635Google Scholar
  88. Patrick-Iwuanyanwu KC, Onyeike EN, Adhikari A (2014) Isolation, identification and characterization of gallic acid derivatives from leaves of Tapinanthus bangwensis. J Nat Prod 7:14–19Google Scholar
  89. Raoelison EG, Rafamantanana MH, Razafindrazaka R, Randriantsoa A, Urverg-Ratsimamanga S, Morel N, Quetin-Leclercq J (2013) Vasorelaxant alkaloids from Spirospermum penduliflorum (Menispermaceae), a plant used to treat hypertension in malagasy traditional medicine. Nat Prod Commun Int J Commun Rev 8:575–578Google Scholar
  90. Ratsimamanga-Urverg S, Rasoanaivo P, Ramiaramanana L, Milijaona R, Rafatro H, Verdier F, Rakoto-Ratsimamanga A, Le Bras J (1992) In vitro antimalarial activity and chloroquine potentiating action of two bisbenzylisoquinoline enantiomer alkaloids isolated from Strychnopsis thouarsii and Spirospermum penduliflorum. Planta Med 58:540–543. doi: 10.1055/s-2006-961545 PubMedCrossRefGoogle Scholar
  91. Rodvold KA, McConeghy KW (2014) Methicillin-resistant Staphylococcus aureus therapy: past, present, and future. Clin Infect Dis 58:S20–S27. doi: 10.1093/cid/cit614 PubMedCrossRefGoogle Scholar
  92. Russell KM, Molan PC, Wilkins AL, Holland PT (1990) Identification of some antibacterial constituents of New Zealand manuka honey. J Agric Food Chem 38:10–13. doi: 10.1021/jf00091a002 CrossRefGoogle Scholar
  93. Sandora TJ, Goldmann DA (2012) Preventing lethal hospital outbreaks of antibiotic-resistant bacteria. N Engl J Med 367:2168–2170. doi: 10.1056/NEJMp1212370 PubMedCrossRefGoogle Scholar
  94. Santiago C, Pang EL, Lim K-H, Loh H-S, Ting KN (2014) Reversal of ampicillin resistance in MRSA via inhibition of penicillin-binding protein 2a by Acalypha wilkesiana. BioMed Res Int. doi: 10.1155/2014/965348 Google Scholar
  95. Sarker SD, Nahar L, Kumarasamy Y (2007) Microtitre plate-based antibacterial assay incorporating resazurin as an indicator of cell growth, and its application in the in vitro antibacterial screening of phytochemicals. Methods Nat Prod Res 42:321–324. doi: 10.1016/j.ymeth.2007.01.006 Google Scholar
  96. Schmelzer GH, Gurib-Fakim A (2008) Ressources végétales de l’Afrique tropicale 11 (1): Plantes médicinales. Schmelzer G.H & Gurib-Fakim A, Pay-BasGoogle Scholar
  97. Shibata H, Kondo K, Katsuyama R, Kawazoe K, Sato Y, Murakami K, Takaishi Y, Arakaki N, Higuti T (2005) Alkyl gallates, intensifiers of β-lactam susceptibility in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 49:549–555. doi: 10.1128/AAC.49.2.549-555.2005 PubMedCentralPubMedCrossRefGoogle Scholar
  98. Shimizu M, Shiota S, Mizushima T, Ito H, Hatano T, Yoshida T, Tsuchiya T (2001) Marked potentiation of activity of β-lactams against methicillin-resistant Staphylococcus aureus by corilagin. Antimicrob Agents Chemother 45:3198–3201. doi: 10.1128/AAC.45.11.3198-3201.2001 PubMedCentralPubMedCrossRefGoogle Scholar
  99. Shiota S, Shimizu M, Mizushima T, Ito H, Hatano T, Yoshida T, Tsuchiya T (1999) Marked reduction in the minimum inhibitory concentration (MIC) of beta-lactams in methicillin-resistant Staphylococcus aureus produced by epicatechin gallate, an ingredient of green tea (Camellia sinensis). Biol Pharm Bull 22:1388–1390PubMedCrossRefGoogle Scholar
  100. Shiota S, Shimizu M, Mizusima T, Ito H, Hatano T, Yoshida T, Tsuchiya T (2000) Restoration of effectiveness of β-lactams on methicillin-resistant Staphylococcus aureus by tellimagrandin I from rose red. FEMS Microbiol Lett 185:135–138. doi: 10.1111/j.1574-6968.2000.tb09051.x PubMedGoogle Scholar
  101. Shiota S, Shimizu M, Sugiyama J, Morita Y, Mizushima T, Tsuchiya T (2004) Mechanisms of action of corilagin and tellimagrandin I that remarkably potentiate the activity of beta-lactams against methicillin-resistant Staphylococcus aureus. Microbiol Immunol 48:67–73PubMedCrossRefGoogle Scholar
  102. Sibanda T, Okoh AI (2007) The challenges of overcoming antibiotic resistance: plant extracts as potential sources of antimicrobial and resistance modifying agents. Afr J Biotechnol. doi: 10.4314/ajb.v6i25.58241 Google Scholar
  103. Sofidiya MO, Jimoh Florence O, Aliero Adamu A, Afolayan Anthony J, Odukoya Olukemi A, Familoni Oluwole B (2012) Evaluation of antioxidant and antibacterial properties of six Sapindaceae members. J Med Plants Res. doi: 10.5897/JMPR11.1364 Google Scholar
  104. Sonibare M, Soladoye M, Esan O, Sonibare O (2009) Phytochemical and antimicrobial studies of four species of Cola Schott & Endl. (Sterculiaceae). Afr J Tradit Complement Altern Med 6:518–525PubMedCentralPubMedGoogle Scholar
  105. Stapleton PD, Shah S, Anderson JC, Hara Y, Hamilton-Miller JMT, Taylor PW (2004) Modulation of β-lactam resistance in Staphylococcus aureus by catechins and gallates. Int J Antimicrob Agents 23:462–467. doi: 10.1016/j.ijantimicag.2003.09.027 PubMedCrossRefGoogle Scholar
  106. Stapleton PD, Shah S, Ehlert K, Hara Y, Taylor PW (2007) The β-lactam-resistance modifier (–)-epicatechin gallate alters the architecture of the cell wall of Staphylococcus aureus. Microbiol Read Engl 153:2093–2103. doi: 10.1099/mic.0.2007/007807-0 CrossRefGoogle Scholar
  107. Stevigny C, Block S, De Pauw-Gillet MC, de Hoffmann E, Llabrès G, Adjakidjé V, Quetin-Leclercq J (2002) Cytotoxic aporphine alkaloids from Cassytha filiformis. Planta Med 68:1042–1044. doi: 10.1055/s-2002-35651 PubMedCrossRefGoogle Scholar
  108. Stévigny C, Block S, De Pauw-Gillet MC, de Hoffmann E, Llabrès G, Adjakidjé V, Quetin-Leclercq J (2002) Cytotoxic aporphine alkaloids from Cassytha filiformis. Planta Med 68:1042–1044. doi: 10.1055/s-2002-35651 PubMedCrossRefGoogle Scholar
  109. Surup F, Medjedović A, Szczygielski M, Schroers H-J, Stadler M (2014) Production of trichothecenes by the apple sooty blotch fungus Microcyclospora tardicrescens. J Agric Food Chem 62:3525–3530. doi: 10.1021/jf500153d PubMedCrossRefGoogle Scholar
  110. Tagne RS, Telefo BP, Nyemb JN, Yemele DM, Njina SN, Goka SMC, Lienou LL, Nwabo Kamdje AH, Moundipa PF, Farooq AD (2014) Anticancer and antioxidant activities of methanol extracts and fractions of some Cameroonian medicinal plants. Asian Pac J Trop Med 7(S1):S442–S447. doi: 10.1016/S1995-7645(14)60272-8 CrossRefGoogle Scholar
  111. Tanko Y, Yaro AH, Isa AI, Yerima M, Saleh MIA, Mohammed A (2007) Toxicological and hypoglycemic studies on the leaves of Cissampelos mucronata (Menispermaceae) on blood glucose levels of streptozocin-induced diabetic wistar rats. J Med Plants Res 1:113–116Google Scholar
  112. Tapondjou LA, Nyaa LBT, Tane P, Ricciutelli M, Quassinti L, Bramucci M, Lupidi G, Ponou BK, Barboni L (2011) Cytotoxic and antioxidant triterpene saponins from Butyrospermum parkii (Sapotaceae). Carbohydr Res 346:2699–2704. doi: 10.1016/j.carres.2011.09.014 PubMedCrossRefGoogle Scholar
  113. Taylor PW (2013) Alternative natural sources for a new generation of antibacterial agents. Int J Antimicrob Agents 42:195–201. doi: 10.1016/j.ijantimicag.2013.05.004 PubMedCrossRefGoogle Scholar
  114. Tchiapke L, Balansard G, Bernard P, Placidi M (1980) Chemical and toxicological study of Anchomanes difformis (Engl). Herba Hung 19:55–63Google Scholar
  115. Tenover FC (2006) Mechanisms of antimicrobial resistance in bacteria. Am J Med 119:S3–S10. doi: 10.1016/j.amjmed.2006.03.011 PubMedCrossRefGoogle Scholar
  116. Tshibangu JN, Wright AD, König GM (2003) HPLC isolation of the anti-plasmodially active bisbenzylisoquinone alkaloids present in roots of Cissampelos mucronata. Phytochem Anal 14:13–22. doi: 10.1002/pca.673 PubMedCrossRefGoogle Scholar
  117. Udegbunam SO, Udegbunam RI, Okpo OS, Muogbo CJ (2012) Evaluation of the wound healing potential of Protea madiensis olive leaf extract in rats. Afr J Biotechnol 11:15719–15727. doi: 10.5897/AJB12.517 CrossRefGoogle Scholar
  118. Wagner H, Bladt S (1996) Plant drug analysis: a thin layer chromatography atlas. Springer, BerlinCrossRefGoogle Scholar
  119. Yemoa A, Gbenou J, Affolabi D, Moudachirou M, Bigot A, Anagonou S, Portaels F, Martin A, Quetin-Leclercq J (2014) Beninese medicinal plants as a source of antimycobacterial agents: bioguided fractionation and in vitro activity of alkaloids isolated from Holarrhena floribunda used in traditional treatment of buruli ulcer. BioMed Res Int. doi: 10.1155/2015/835767 Google Scholar
  120. Yotis W, Stanke R (1966) Bacteriostatic action of progesterone on Staphylococci and other microorganisms. J Bacteriol 92:1285–1289PubMedCentralPubMedGoogle Scholar
  121. Yu H-H, Kim K-J, Cha J-D, Kim H-K, Lee Y-E, Choi N-Y, You Y-O (2005) Antimicrobial activity of berberine alone and in combination with ampicillin or oxacillin against methicillin-resistant Staphylococcus aureus. J Med Food 8:454–461. doi: 10.1089/jmf.2005.8.454 PubMedCrossRefGoogle Scholar
  122. Zerbo P, Millogo-Rasolodimby J, Nacoulma-Ouedraogo OG, Van Damme P (2011) Plantes médicinales et pratiques médicales au Burkina Faso : cas des Sanan. Bois For Trop 1:41–53Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  1. 1.Louvain Drug Research InstituteUniversité catholique de LouvainWoluwe-Saint-LambertBelgium

Personalised recommendations