In Vitro antibacterial and antibiotic-potentiation activities of four edible plants against multidrug-resistant gram-negative species

BMC Complementary and Alternative Medicine

Victor Kuete²  Jean P Dzoyem²  Dumitru Cojocaru¹  Marius Stefan¹  Jules R Kuiate²  Marius Mihasan¹  Jaurès AK Noumedem¹ 

[1] Department of Biochemistry and Molecular Biology, Faculty of Biology, University ALI Cuza, Iasi, Romania;Department of Biochemistry, Faculty of Science, University of Dschang, Dschang, Cameroon

关键词: Efflux pumps;    Multidrug resistance;    Gram-negative bacteria;    Edible plants;    Antibacterial activities;   

Others  :  1221056
DOI  :  10.1186/1472-6882-13-190

 received in 2013-03-07, accepted in 2013-07-24,  发布年份 2013

【 摘 要 】

Background

The present study was designed to investigate the antibacterial activities of the methanol extracts of four Cameroonian edible plants, locally used to treat microbial infections, and their synergistic effects with antibiotics against a panel of twenty nine Gram-negative bacteria including Multi-drug resistant (MDR) phenotypes expressing active efflux pumps.

Methods

The broth microdilution method was used to determine the minimum inhibitory concentrations (MICs) of the extracts [alone and in the presence of the efflux pumps inhibitor (EPI) Phenylalanine-Arginine β-Naphtylamide (PAβN)], and those of antibiotics in association with the two of the most active ones, Piper nigrum and Telfairia occidentalis. The preliminary phytochemical screening of the extracts was conducted according to the standard phytochemical methods.

Results

Phytochemical analysis showed the presence of alkaloids and flavonoids in all studied extracts. Other chemical classes of secondary metabolites were selectively present in the extracts. The results of the MIC determination indicated that the crude extracts from P. nigrum and V. amygdalina were able to inhibit the growth of all the twenty nine studied bacteria within a concentration range of 32 to 1024 μg/mL. At a similar concentration range (32 to 1024 μg/mL) the extract from T. occidentalis inhibited the growth of 93.1% of the tested microorganisms. At MIC/2 and MIC/5, synergistic effects were noted between the extracts from P. nigrum and T. occidentalis and seven of the tested antibiotics on more than 70% of the tested bacteria.

Conclusion

The overall results of the present study provide information for the possible use of the studied edible plants extracts in the control of bacterial infections including MDR phenotypes.

【 授权许可】

   
2013 Noumedem et al.; licensee BioMed Central Ltd.

【 参考文献 】

• [1]Ahluwalia G, Sharma SK: Philanthropy and medical science: at last a new dawn for tuberculosis also! Indian J Chest Dis Allied Sci 2007, 49:71-73.
• [2]Adwan G, Abu-Shanab B, Adwan K: Antibacterial activities of some plant extracts alone and in combination with different antimicrobials against multidrug-resistant Pseudomonas aeruginosa strains. Asian Pac J Trop Med 2010, 3(4):266-269.
• [3]Poole K: Efflux-mediated antimicrobial resistance. J Antimicrob Chemother 2005, 56:20-51.
• [4]Ates DA, Erdogrul OT: Antimicrobial activity of various medicinal and commercial plants extracts. Turk J Biol 2003, 27:157-162.
• [5]Rahman S, Parvez AK, Islam R, Khan MH: Antibacterial activity of natural spices on multiple drug resistant Escherichia coli isolated from drinking water Bangladesh. Ann Clin Microbiol Antimicrob 2011, 10:10. BioMed Central Full Text
• [6]Newman DJ, Cragg GM: Natural products as sources of new drugs over the last 25 years. J Nat Prod 2007, 70(3):461-477.
• [7]Coutinho HDL, Siqueira-Júnior JG, JP : Additive effects of Hyptis martiusii Benth with aminoglycosides against Escherichia coli. Indian J Med Res 2010, 131:106-108.
• [8]Nisar A, Fazal H, Abbasi BH, Farooq S, Ali M, Khan MA: Biological role of Piper nigrum L. (Black pepper): a review. Asian Pac J Trop Biomed 2012, 2(3):S1945-S1953.
• [9]Menon AN, Padmakumari KP, Jayalekshmy A: Essential oil composition of four major cultivars of Black Pepper (Piper nigrum L) III. J Essent Oil Res 2003, 15(3):155-157.
• [10]Kang MJ, Cho JYS, Duk K, Kim BH, Lee J: Bioavailability enhancing activities of natural compounds from medicinal plants. J Med Plant Res 2009, 3(13):1204-1211.
• [11]Ee GCL, Lim CM, Rahmani M, Shaari K, Bong CFJ: Pellitorine, a potential Anti-cancer lead compound against HL60 and MCT-7 cell lines and microbial transformation of piperine from Piper nigrum. Molecules 2010, 15(4):2398-2404.
• [12]Vijayakumar RS, Surya D, Nalini N: Antioxidant efficacy of black pepper (Piper nigrum L.) and piperine in rats with high fat diet induced oxidative stress. Redox Rep 2004, 9(2):105-110.
• [13]Neha JMR: Antioxidant activity of Trikatu megaExt. Inter J Res Pharm Biomed Sci 2011, 2(2):624-628.
• [14]Erturk O: Antibacterial and antifungal activity of ethanolic extracts from eleven spice plants. Biologia Bratisl 2006, 61(3):275-278.
• [15]Li S, Wang C, Li W, Koike K, Nikaido T, Wang MW: Antidepressant-like effects of Piperine and its derivative, antiepilepsirine. J Asian Nat Prod Res 2007, 9:421-430.
• [16]Umit AK, Akgun KO: Antifungal activity of aqueous extracts of spices against bean rust (Uromyces appendiculatus). Allelopathy J 2009, 24:0973-5046.
• [17]Parmar VS, Bracke ME, Philippe J, Wengel J, Jain SC, Olsen CE, Bisht KS, Sharma NK, Courtens A, Sharma SK, Vennekens K, Van Marck V, Singh SK, Kumar N, Kumar A, Malhotra S, Kumar R, Rajwanshi VK, Jain R, Mareel MM: Anti-invasive activity of alkaloids and polyphenolics in vitro. Bioorg Med Chem 1997, 5(8):1609-1619.
• [18]Kumar S, Singhal V, Roshan R, Sharma A, Rembhotkar GW, Ghosh B: Piperine inhibits TNF- α induced adhesion of neutrophils to endothelial monolayer through suppression of NF-κ and IκB kinase activation. Eur J Pharmacol 2007, 575:177-186.
• [19]Pathak N, Khandelwal S: Cytoprotective and immunomodulating properties of piperine on murine splenocytes: an in vitro study. Eur J Pharmacol 2007, 576(1–3):160-170.
• [20]Sunila ES, Kuttan G: Immunomodulatory and antitumor activity of Piper longum Linn. and piperine. J Ethnopharmacol 2004, 90(2–3):339-346.
• [21]Upadhyay RK, Jaiswal G: Evaluation of biological activities of Piper nigrum oil against Tribolium castaneum. Bull Insectology 2007, 60:57-61.
• [22]Tajuddin Ahmad S, Latif A, Qasmi I: Effect of 50% ethanolic extract of Syzygium aromaticum (L.) Merr. & Perry. (clove) on sexual behaviour of normal male rats. BMC Complement Altern Med 2004, 4(1):17. BioMed Central Full Text
• [23]Sharma A, Kumar M, Kaur S: Modulatory effects of Syzygium aromaticum (L.) Merr. & Perry and Cinnamomum tamala Nees & Ebrem. on toxicity induced by chromium trioxide. Phytopharmacology 2011, 1(4):71-81.
• [24]Moleyar V, Narasimham P: Antibacterial activity of essential oil components. Int J Food Microbiol 1992, 16(4):337-342.
• [25]Palombo E: Traditional medicinal plant extracts and natural products with activity against oral bacteria: potential application in the prevention and treatment of oral diseases. eCAM 2011, 2011:680354.
• [26]Pinto E, Vale-Silva L, Cavaleiro C, Salgueiro L: Antifungal activity of the clove essential oil from Syzygium aromaticum on Candida, Aspergillus and dermatophyte species. J Med Microbiol 2009, 58:1454-1462.
• [27]Wagner H, Jurcic K, Deininger R: Über die spasmolytische Wirkung von Eugenolestern und -äthern. Planta Med 1979, 37(09):9,14.
• [28]Banerjee S, Das S: Anticarcinogenic Effects of an aqueous infusion of cloves on skin carcinogenesis. Asia Pacific J Cancer Prev 2005, 6(3):304-308.
• [29]Fregni V, Casadio R: Kinetic characterization of the ATP-dependent proton pumps in bacterial photosynthetic membranes: a study with the fluorescent probe 9-amino-6-chloro-2-methoxyacridine. BBA - Bioenergetics 1993, 1143(2):215-222.
• [30]Pandey A, Singh P: Antibacterial activity of Syzygium aromaticum (clove) with metal ion effect against food borne pathogens. Asia J Plant Sci 2011, 1(2):69-80.
• [31]Eseyin OA, Ebong P, Ekpo A, Igboasoiyi A, Oforah E: Hypoglycemic effect of the seed extract of Telfairia occidentalis in rat. Pakistan J Biol Sci 2007, 10(3):498-501.
• [32]Oboh G, Nwanna EE, Elusiyan CA: Antioxidant and antimicrobial properties of Telfairia occidentalis (Fluted pumpkin) leaf extracts. J Pharmacol Toxicol 2006, 1(2):167-175.
• [33]Kayode AAA, Kayode OT, Odetola AA: Telfairia occidentalis ameliorates oxidative brain damage in Malnorished rats. nt J Biol Sci 2010, 4(1):10-18.
• [34]Iwalokun BB, SB , Durojaiye OO: An Antimicrobial Evaluation of Vernonia amygdalina (Compositae) against Gram - positive and Gram-Negative bacteria from Lagos, Nigeria. W Afr J Pharmacol Drug Res 2003, 19:9-15.
• [35]Uzoigwe CA, OK : Antimicrobial activity of Vernonia amygdalina on selected urinary tract pathogens. Afr J Microbiol Res 2011, 5(12):1467-1472.
• [36]Akinpelu DA: Antimicrobial activity of Vernonia amygdalina leaves. Fitoterapia 1999, 70(4):432-434.
• [37]Nwanjo HU, Nwokoro EA: Antidiabetic and biochemical effects of aqueous extract of Vernonia amygdalina leaf in normoglycaemic and and diabetic rats. J Innov Life Sci 2004, 7:6-10.
• [38]Kupchan SM, Hemingway RJ, Karim A, Werner D: Tumor inhibitors. XLVII. Vernodalin and vernomygdin, two new cytotoxic sesquiterpene lactones from Vernonia amygdalina Del. J Organic Chem 1969, 34(12):3908-3911.
• [39]Izevbigie EB: Discovery of water soluble anticancer agents from a vegetable found in Benin City, Nigeria. Exp Biol Med 2003, 228:293-298.
• [40]Tadesse A, Gebre-Hiwot A, Asres K, Djote M, Frommel D: The in-vitro activity of Vernonia amygdalina on Leishmania acthiopica. Ethiop Med J 1993, 31:183-189.
• [41]Fasola TO, Okeocha PC, Odetola A: Screening for hypoglycaemic potential of Vernonia amygdalina. Ethnobotanical Leaflets 2010, 14:759-765.
• [42]Ibrahim TA, Ajala L, Adetuyi FO, Jude-Ojei B: Assessment of the antibacterial activity of Vernonia amygdalina and Occimum gratissimum leaves on selected food borne pathogens. Elec J Env Agricult Food Chem 2009, 8(11):1212-1218.
• [43]Nwanjo HU: Efficacy of aqueous leaf extract of Vernonia amygdalina on plasma lipoprotein and oxidative status in diabetic rat models. Niger J Physiol Sci 2005, 20(1–2):39-42.
• [44]Harbone JB: Phytochemical methods: A guide to modern techniques of plant analysis. London: Chapman and Hall; 1973.
• [45]Eloff JN: A sensitive and quick microplate method to determine the minimal inhibitory concentration of plant extracts for bacteria. Planta Med 1998, 64:711-713.
• [46]Mativandlela SPN, Lall N, Meyer JJM: Antibacterial, antifungal and antitubercular activity of Pelargonium reniforme (CURT) and Pelargonium sidoides (DC) (Geraniaceae) root extracts. S Afr J Bot 2006, 72:232-237.
• [47]Kuete V, Ngameni B, Simo CCF, Tankeu RK, Ngadjui BT, Meyer JJM, Lall N, Kuiate JR: Antimicrobial activity of the crude extracts and compounds from Ficus chlamydocarpa and Ficus cordata (Moraceae). J Ethnopharmacol 2008, 120(1):17-24.
• [48]Shahverdi AR, Monsef-Esfahani HR, Tavasoli F, Zaheri A, Mirjani R: Trans-Cinnamaldehyde from Cinnamomum zeylanicum Bark Essential Oil Reduces the Clindamycin Resistance of Clostridium difficile in vitro. J Food Sci 2007, 72(1):S055-S058.
• [49]Braga LC, Leite AAM, Xavier KGS, Takahashi JA, Bemquerer MP, Chartone-Souza E, Nascimento AMA: Synergic interaction between pomegranate extract and antibiotics against Staphylococcus aureus. Can J Microbiol 2005, 51(7):541-547.
• [50]Cowan MM: Plant products as antimicrobial agents. Clin Microbiol Rev 1999, 12(4):564-582.
• [51]Kuete V: Potential of Cameroonian plants and derived products against microbial infections: a review. Planta Med 2010, 76(EFirst):1479-1491.
• [52]Karaman İ, Şahin F, Güllüce M, Öǧütçü H, Şengül M, Adıgüzel A: Antimicrobial activity of aqueous and methanol extracts of Juniperus oxycedrus L. J Ethnopharmacol 2003, 85(2–3):231-235.
• [53]Ono T, Kashimura M, Suzuki K, Oyauchi R, Miyachi J, Ikuta H, Kawauchi H, Akashi T, Asaka T, Morimoto S: In vitro and in vivo antibacterial activities of the tricyclic ketolide te-802 and its analogues. J Antibiot (Tokyo) 2004, 57(8):518-527.
• [54]Pavithra VK, O Bhagya L: Antibacterial activity of black pepper (Piper nigrum Linn.) with special reference to its mode of action bacteria. Indian J Comp Microbiol Immunol Infect Dis 2009, 30(1):65-66.
• [55]Blot S, Depuydt P, Vandewoude K, De-Bacquer D: Measuring the impact of multidrug resistance in nosocomial infection. Curr Opin Infect Di 2007, 20:391-396.
• [56]Papadopoulos CJCC, Chang BJ: Role of the MexAB-OprM efflux pump of Pseudomonas aeruginosa in tolerance to tea tree (Melaleuca alternifolia) oil and its monoterpene components terpinen-4-ol, 1,8-cineole and α-terpineol. Appl Environ Microbiol 2008, 74:1932-1935.
• [57]Lomovskaya O, Bostian KA: Practical applications and feasibility of efflux pump inhibitors in the clinic–a vision for applied use. Biochem Pharmacol 2006, 71:910-918.
• [58]Pages J-M, Lavigne J-P, Leflon-Guibout V, Marcon E, Bert F, Noussair L, Nicolas-Chanoine M-H: Efflux Pump, the Masked Side of ß-Lactam Resistance in Klebsiella pneumoniae clinical isolates. PLoS One 2009, 4(3):e4817.
• [59]Lorenzi V, Muselli A, Bernardini AF, Berti L, Pagès JM, Amaral L, Bolla JM: Geraniol restores antibiotic activities against multidrug-resistant isolate from Gram-negative species. Antimicrob Agents Chemother 2009, 53:2209-2211.