Skip to main content
  • Research article
  • Open access
  • Published:

Antibacterial activities of the methanol extracts of ten Cameroonian vegetables against Gram-negative multidrug-resistant bacteria

Abstract

Background

Many edible plants are used in Cameroon since ancient time to control microbial infections. This study was designed at evaluating the antibacterial activities of the methanol extracts of ten Cameroonian vegetables against a panel of twenty nine Gram negative bacteria including multi-drug resistant (MDR) strains.

Methods

The broth microdilution method was used to determine the Minimal Inhibitory Concentrations (MIC) and the Minimal Bactericidal Concentrations (MBC) of the studied extracts. When chloramphenicol was used as a reference antibiotic, the MICs were also determined in the presence of Phenylalanine-Arginine β- Naphtylamide (PAβN), an efflux pumps inhibitor (EPI). The phytochemical screening of the extracts was performed using standard methods.

Results

All tested extracts exhibited antibacterial activities, with the MIC values varying from 128 to 1024 mg/L. The studied extracts showed large spectra of action, those from L. sativa, S. edule, C. pepo and S. nigrum being active on all the 29 bacterial strains tested meanwhile those from Amaranthus hybridus, Vernonia hymenolepsis, Lactuca.carpensis and Manihot esculenta were active on 96.55% of the strains used. The plant extracts were assessed for the presence of large classes of secondary metabolites: alkaloids, anthocyanins, anthraquinones, flavonoids, phenols, saponins, steroids, tannins and triterpenes. Each studied plant extract was found to contain compounds belonging to at least two of the above mentioned classes.

Conclusion

These results confirm the traditional claims and provide promising baseline information for the potential use of the tested vegetables in the fight against bacterial infections involving MDR phenotypes.

Peer Review reports

Background

Infectious diseases are still a major health concern, accounting for 41% of the global disease burden measured in terms of Disability-Adjusted Life Years (DALYS), close to all noninfectious diseases (43%) and far more than injuries (16%) [1]. One of the main causes of this problem is the widespread emergence of acquired bacterial resistance to antibiotics in such a way that the world is facing today, a serious threat to global public health [2] in the form of not only epidemics, but also pandemics of antibiotic resistance [3]. Several mechanisms have been accounted for, but active efflux plays an important role in this phenomenon [4]. The accumulation of different antibiotic resistance mechanisms within the same strains has led to the appearance of the so called superbugs, or multi-drug resistant bacteria [2]. Due to this problem of resistance to antibiotics, attention is now being shifted towards biologically active components isolated from plant species commonly used as herbal medicine, as they may offer a new source of antibacterial, antifungal and antiviral activities [5]. The potential antimicrobial properties of plants are related to their ability to synthesize several secondary metabolites of relatively complex structures possessing antimicrobial activities [6, 7]. Among medicinal plants, vegetables associated to non or less-toxic effects have been shown to possess many medicinal properties [8, 9] including antibacterial effects [3]. The present work was therefore designed to investigate the antibacterial effects of ten Cameroonian vegetables namely Amarantus hybridus Linn (Amarantaceae), Vernonia hymenolepis (H.F.) Hook., Lactuca sativa Linn. and Lactuca capensis Thumb. (Asteraceae), Manihot esculenta Crantz (Euphorbiaceae), Phaseolus vulgaris Linn (Fabaceae), Cucurbita pepo Linn and Sechium edule (Jacq) Sw. (Cucurbitaceae), Solanum nigrum Linn. and Capsicum frutescens L. (Solanaceae) against MDR bacteria expressing active efflux pumps

Methods

Plant material and extraction

The collected plant materials used in this study were harvested from Dschang, West Region of Cameroon in June 2010 and included the leaves of Amarathus hybridus, Vernonia hymenolepis, Lactuca sativa, Lactuca capensis, Sechium edule, Manihot esculenta, Curcubiata pepo, Solanum nigrum, the cloves of the Green bean (Phaseolus vulgaris), and the fruits of Capsicum frutescens. These plants were identified by Mr Victor Nana of the National Herbarium (Yaoundé-Cameroon) where all the voucher specimens were deposited with the corresponding reference number (Table 1).

Table 1 Plant species used in this study and their reported effects

Air dried and powdered sample (1 kg) of each plant was extracted with methanol (MeOH) for 48 h at room temperature (25°C), using Whatman Grade No.1 filter paper and concentrated under reduced pressure, then dried to give the crude extracts. All extracts were stored at 4°C until further use.

Preliminary phytochemical investigations

The major secondary metabolites classes such as alkaloids, anthocyanins, anthraquinones, flavonoids, phenols, saponins, tannins, sterols and triterpenes were screened according to the common phytochemical methods previously described by Harbone, 1973 [70].

Bacterial strains and culture media

The studied bacteria included both reference (from the American Type Culture Collection) and clinical strains of Providencia stuartii, Pseudomonas aeruginosa, K. pneumoniae, Escherichia coli, Enterobacter aerogenes and Enterobacter cloacae (See Additional file 1: Table S1 for their features). These clinical strains were obtained from the laboratory “Transporteurs Membranaires, Chimiorésistance et Drug Design, UMR-MD1, IFR 88, UFRs de Médecine et de Pharmacie, Marseille, France”. All strains were maintained in Nutrient Broth at 4°C and activated on Mueller Hinton Agar plates 24 h prior to any antimicrobial test. Mueller Hinton Broth (MHB) was used for all antibacterial assays.

Bacterial susceptibility testing

The MICs were determined using the rapid INT colorimetric assay [71, 72]. Briefly, test samples were first emulsified in DMSO/MHB (50:50 V/V). The solution obtained was then added to MHB, and serially diluted two fold (in a 96- wells microplate). One hundred microlitres (100 μl) of inoculum (1.5 × 106 CFU/ml) prepared in MHB was then added. The plate was covered with a sterile plate sealer, then agitated to mix the contents of the wells using a shaker and incubated at 37°C for 18 h. The final concentration of DMSO was 2.5% and did not affected the microbial growth. Wells containing MHB, 100 μl of inoculum and DMSO at a final concentration of 2.5% served as negative control. The MICs of samples were detected after 18 h incubation at 37°C, following addition of 40 μl of a 0.2 mg/ml INT solution and incubation at 37°C for 30 minutes. Viable bacteria reduce this yellow dye to pink. MIC was defined as the lowest sample concentration that exhibited complete inhibition of microbial growth and then prevented this change [73]. The MBC was determined by adding 50 μL of the suspensions from the wells, which did not show any growth after incubation during MIC assays, to 150 μL of fresh broth. These suspensions were re-incubated at 37°C for 48 hours. The MBC was determined as the lowest concentration of extract which completely inhibited the growth of bacteria [74].

Chloramphenicol, used as reference antibiotic, was tested also in the presence of the PAβN, at 30 mg/L final concentration to confirm the resistance of bacterial strains.

Results

Chemical composition of the vegetable extracts

The results of the qualitative analysis showed that each of the studied plant extract contains at least two classes of secondary metabolites such as alkaloids, anthocyanins, anthraquinones, flavonoids, phenols, saponins, steroids, tannins and triterpenes (Table 2). Only the extract from A. hybridus contains anthocyanins, while triterpenes were found both in this extract as well as that of C. frutescens. The extract from C. frutescens as well as those from S. edule and M. esculenta contained the highest number of classes of the studied secondary metabolites (five). Alkaloids and phenols were present in all vegetable extracts except that of A. hybridus.

Table 2 Extraction yields and phytochemical composition of the plant extracts

Antibacterial activity of the vegetable extracts

The data summarized in Table 3 show the antibacterial activities of the tested extracts on a panel of twenty-nine Gram-negative bacteria. All extracts were active on at least twelve bacterial strains with MIC ≤ 1024 μg/ml. The extract of C. frutescens showed inhibitory activities against 16 (55.17%) of the 29 tested bacteria whilst that of P. vulgaris inhibited the growth of 12/29 (41.38%) pathogens (narrowest spectrum). None of these two extracts showed any antibacterial activity against Pseudomonas species, but were active against at least one bacterial strain of other studied genus. Extracts from L. sativa, S. edule, C. pepo and S. nigrum displayed the largest spectra of activity, their inhibitory effects being observed on all the 29 Gam-negative bacteria (100% of activity). The extracts from A. hybridus, V. hymenolepis, L. sativa, L. carpensis and M. esculenta also exhibited large spectrum of activity as they were active on 28/29 tested bacteria. The top eight active extracts, with large spectra of activity, showed MIC values generally ranging from 128 to 512 μg/ml. These MIC values were in some of the cases better than those of choramplenicol (Table 3). This was the case with the extract from V. hymenolepis (MIC of 128 μg/ml) against E. aerogenes EA27. The extracts from A. hybridus, S. edule and C. pepo as well as those from L. capensis and M. esculenta were more active than chloramphenicol on at least one of the tested MDR bacteria. The activity of chloramphenicol increased in the presence of PAβN in the majority of the tested bacteria (Table 3). The best activity was obtained with the extract from A. hybridus with the lowest MIC value of 128 μg/ml observed against 7/29 (25%) tested bacteria. The extracts from P. vulgaris and C. frutescens did not show any MBC value at up to 1024 μg/ml. Concering the eight other vegetable extracts, the MBC results showed values equal to or below 1024 μg/ml in many cases. The extract from C. pepo leaves showed the best MBC spectrum with the values below to 1024 μg/ml recorded on 58,62% (17/29) of the studied microorganisms, followed by those from M. esculenta leaves on 51,72% (15/29), A. hybridus, V. hymenolepis and L. capensis extracts on 44.83% (13/29) and L. sativa on 31.03% (9/29) (Table 4).

Table 3 Susceptibility of bacteria to plant extracts - MICs of methanol extracts vs chloramphenicol
Table 4 Susceptibility of bacteria to plant extracts - MBCs (μg/ml) of methanol extracts vs chloramphenicol

Table 4 also shows that M. esculenta exhibited MBC values against all the strains of E. aerogenes and that, in general, the extracts showed values which were not 4-fold greater than the corresponding MICs.

Discussion

In plants, secondary metabolites attract beneficial and repel harmful organisms, serve as phytoprotectants and respond to environmental changes. In animals, such compounds have many beneficial effects including antibacterial and antiviral properties [75, 76]. The classes of secondary metabolites detected in the tested vegetables can somehow provide a prelimanry explanation on their activities [77]. In general, the phytochemical contents (Table 2) were in accordance with the previous reports for some of the vegetables where data were available [11, 12, 23, 38]. It should however be mentioned that the detection of the bioactive phytochemical classes in a plant is not a guarantee for any biological property, as this will depend on the types of compounds, as well as their concentrations and possible interaction with other constituents.

Solanum nigrum has been shown to possess various activities such as antitumorigenic, antioxidant, anti-inflammatory, hepatoprotective diuretic and antipyretic [63]. Though the exact mechanism of action remains to be elucidated in many cases, few are known about its antibacterial properties. In fact, it has been shown that seeds of S. nigrum possess good antimicrobial activity against E. coli on solid medium [63]. We report herein for the first time the antibacterial activity of leaves methanol extract of this plant against a panel of MDR Gram-negative bacterial strains with MIC values varying from 128 to 1024 μg/ml (Table 3). Solanum nigrum possesses various compounds that are responsible for diverse activities. Among these compounds, solanine (found in all parts of the plant [58]),is its major defence product [58].

Many reports have also been published about the biological properties of C. pepo, but these reports are based on the components of the fruits and the seed’s oil [54, 55, 57, 78]. To the best of our knowledge, were herein report for the first time its activities against MDR bacteria.

The results of the phytochemical test on P. vulgaris are in accordance with some other reports [48, 79]. Phaseolus vulgaris was found to inhibit also the growth of Gram-positive bacteria B.subtilis[49]. Amarowicz et al. [80] showed that the acetone extract of P. vulgaris contains tannins with good antimicrobial properties against Listeria monocytogenes. Therefore, the low antibacterial effects of this plant as obtained herein (generally MIC values at 1024 μg/ml) (Table 3) could be due to the multi-drug resistance ability of the studied bacteria.

The antibacterial effects of the extract from C. frutescens against Staphylococcus aureus as well as K. pneumoniae and P. aeruginosa have been reported [67]. The ethanol extract of this plant was also active against MDR strains of S. aureus[81]. The present study therefore provides additional information on the antibacterial potential of this plant on MDR Gram-negative bacteria with MICs ranging from 256 to 024 μg/ml.

The antibacterial properties of S. edule have already been proved against bacteria of clinical relevance by Ordonez et al. [41] which showed that both fluid extract and tincture of fruits have “very good antimicrobial activities against MDR staphylococci and enterococci [41]. Herein, the antimicrobial activity of the leaves extract {known to possess high level of secondary metabolites and mostly flavonoids [39]} observed against all the studied bacterial strains (Table 3) is being reported for the first time.

The chloroform extract of M. esculenta possess antibacterial activities against Listeria monocytogenes, Vibrio cholerae, Shigella flexneri and Salmonella typhi whilst ethanol extract was found active against P. aeruginosa, Corynebacterium diphtheriae and V. cholera[46]. This report provides additional data on antibacterial activity of M. esculenta against MDR strains of P. aeruginosa, E. coli, E. cloacae, K. pneumoniae, P stuartii and E. aeorogenes. The activity of Amaranthus hybridus was reported against E. coli, S. typhi, K. pneumoniae and P. aeruginosa with MICs ranged between 200 and 755 mg/ml [5]. The ethyl acetate extract exhibited activity against S. aureus and B. subtilis whilst the ethanol extract was found effective against E.coli[13].

The high MIC values observed with chloramphenicol can be explained only if we take into account the non-specific resistance mechanism: active efflux of the toxic compound by pumps belonging to the small multidrug resistance (SMR) proteins family [4]. The fact that the efflux pump inhibitor (PAβN) enhances the chloramphenicol antibacterial properties is a clear indication that the tested strains express an active efflux system and that this system is responsible for resistance of the tested bacteria to chloramphenicol. The wide substrate specificity of these pumps, as well as their widespread among bacterial species make us believe that these efflux pumps are also responsible for the extrusion of various active compounds from the plant extract out of bacteria cells, therefore preventing their inhibitory effects. Therefore, the activities of the vegetable as observed herein against MDR strains (with MIC comprised between 128 and 1024 μg/mL) could be considered important, especially when considering the fact that we are dealing with edible plants. Apart for the extracts of P. vulgaris and C. frutescens which did not show any MBC below 1024 μg/ml, other values further confirmed the bactericidal effect of the 8 remaining extracts as they were generally less than 4-fold greater than corresponding MIC values [82, 83].

Conclusions

The overall results of the present investigation confirmed the traditional uses of the studied vegetables in the treatment of bacterial infections. This study also provide baseline information for the possible use of the methanol extracts of the tested plant samples in the control of infectious diseases involving Gram-negative MDR bacteria. The arising question is of course which are the active compounds responsible for these effects. Our research group is currently focusing on the characterization of these plants extracts in terms of chemical composition and synergistic effects.

References

  1. NIE 99-17D NIE: The global infectious disease threat and its implications for the United States. 2000, http://www.heart-intl.net/HEART/072404/. accessed on August 12, 2012

    Google Scholar 

  2. Chopra I: New drugs for superbugs. Microbiology Today. 2000, 47: 4-6.

    Google Scholar 

  3. Chanda S, Baravalia Y, Kaneria M, Rakholiya K: Fruit and vegetable peels – strong natural source of antimicrobics. Current research, technology and education topics in apllied microbiology and microbial biotechnology. Edited by: Mendez-Vilas A. 2010, Badajoz, Spain: Formatex

    Google Scholar 

  4. 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: e4817-10.1371/journal.pone.0004817.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Maiyo ZC, Ngure RM, Matasyoh JC, Chepkorir R: Phytochemical constituents and antimicrobial activity of leaf extracts of three Amaranthus plant species. Afr J Biotechnol. 2010, 9: 3178-3182.

    Google Scholar 

  6. Matasyoh JC, Maiyo ZC, Ngure RM, Chepkorir R: Chemical composition and antimicrobial activity of the essential oil of Coriandrum sativum. J Food Chem. 2009, 113: 526-529. 10.1016/j.foodchem.2008.07.097.

    Article  CAS  Google Scholar 

  7. Evarando LS, Oliveira LE, Freire LKR, Sousa PC: Inhibitory action of some essential oils and phytochemicals on growth of various moulds isolated from foods. Braz Arch Biol Technol. 2005, 48: 234-241.

    Google Scholar 

  8. Hedges LJ, Lister CE: Nutritional attributes of some exotic and lesser known vegetables. Plant & Food Research Confidential Report No. 2325. 2009, New Zealand Institute for Plant & Food Research Limited

    Google Scholar 

  9. Dhiman K, Gupta A, Sharma DK, Gill NS, Goyal K: A review on the medicinal important plants of the family of Cucurbitaceae. Asian J Clin Nutr. 2012, 4: 16-26. 10.3923/ajcn.2012.16.26.

    Article  CAS  Google Scholar 

  10. He HP, Corke H, Cai JG: Supercritical carbon dioxide extraction of oil and squalene from Amaranthus Grain. J Agr Food Chem. 2003, 51: 7921-7925. 10.1021/jf030488y.

    Article  CAS  Google Scholar 

  11. Akubugwo IE, Obasi NA, Chinyere GC, Ugbogu AE: Nutritional and chemical value of Amaranthus hybridus L. leaves from Afikpo Nigeria. Afr J Biotechnol. 2007, 6 (24): 2833-2839.

    Article  CAS  Google Scholar 

  12. Akubugwo IE, Obasi NA, Chinyere GC, Ugbogu AE: Mineral and phytochemical contents in leaves of Amaranthus hybridus L and Solanum nigrum L. subjected to different processing methods. Afr J Biochem Res. 2008, 2: 040-044.

    Google Scholar 

  13. Dahiya SS, Sheoran SS, Sharma SK: Antibacterial activity of Amaranthus hybridus linn. root extracts. IJABPT. 2010, 1: 46-49.

    Google Scholar 

  14. IeCAB2010: Contribution of agriculture to achieving MDGs. Contribution of Agricultural Sciences towards achieving the Millenium Development Goals. Edited by: Mwangi M. 2010, Kenya: Nairobi, FaCT Publishing

    Google Scholar 

  15. Rajwar S, Khatri P, Patel R, Dwivedi S, Dwivedi A: An overview on potent herbal anticancer drugs. Int J Res Pharm Chem. 2011, 1: 202-210.

    Google Scholar 

  16. Hamisy WC, Mwaseba D, Zilihona IE, Mwihomeke ST: Status and domestication potential of medicinal plants in the Uluguru mountain area, Tanzania. 2000, Morogoro: Tanzania: Wildlife Conservation Society of Tanzania (WCST), 55-

    Google Scholar 

  17. Perdue REJ, Carlson KD, G GM: Vernonia galamensis, potential new crop source of epoxy acid I. Econ Bot. 1986, 40: 54-68. 10.1007/BF02858947.

    Article  CAS  Google Scholar 

  18. Sims RJ: Synthesis of furanosesquiterpenoid natural products. 1981, Southampton: University Of Southampton

    Google Scholar 

  19. Yang R-Y, Lin S, Kuo G: Content and distribution of flavonoids among 91 edible plant species. Asia Pac J Clin Nutr. 2008, 17 (S1): 275-279.

    CAS  PubMed  Google Scholar 

  20. Barrero AF, Oltra JE, Barragán A, Álvarez M: Approaches to the synthesis of 8-epi-vernolepin from germacrolides. J Chem Soc. 1998, 1: 4107-4113.

    Google Scholar 

  21. Fane S: Doctorat d’état. Etude de la toxicite de certaines plantes vendues sur les marches du district de Bamako. 2003, Bamako: Université de Bamako

    Google Scholar 

  22. Bhanu Prasad K, Avinash Kumar RG, Jyothi MJ, Rasheed A, Dalith D: Natural antifilarial drugs: a review. International Journal of Pharmacology and Toxicology. 2011, 1: 1-10.

    Google Scholar 

  23. Rodrigues E, Tabach R, Galduróz JCF, Negri G: Plants with possible anxiolytic and/or hypnotic effects indicated by three Brazilian cultures - Indians, afro-Brazilians, and river-dwellers. Stud Nat Prod Chem. 2008, 35: 549-595.

    Article  CAS  Google Scholar 

  24. Katz SH, Weaver WW: Encyclopidia of food and culture. 2003, New York: In. schribner Ed

    Google Scholar 

  25. Sayyah M, Hadidi N, Kamalinejad M: Analgesic and anti-inflammatory activity of Lactuca sativa seed extract in rats. J Ethnopharmacol. 2004, 92: 325-329. 10.1016/j.jep.2004.03.016.

    Article  PubMed  Google Scholar 

  26. Cruz R, Baptista P, Cunha S, Pereira JA, Casal S: Carotenoids of lettuce (lactuca sativa L.) grown on soil enriched with spent coffee grounds. Molecules. 2012, 17: 1535-1547. 10.3390/molecules17021535.

    Article  CAS  PubMed  Google Scholar 

  27. Van Beek TA, Mass P, King BM, Laclercq E, Voragen AGJ, de Groot A: Bitter sesquiterpene lactones from chicory roots. J Agr Food Chem. 1990, 38: 1035-1038. 10.1021/jf00094a026.

    Article  CAS  Google Scholar 

  28. Brandi G, Amagliani G, Schiavano GF, De Santi M, Sisti M: Activity of Brassica oleracea leaf juice on foodborne pathogenic bacteria. J Food Prot. 2006, 69 (9): 2274-2279.

    CAS  PubMed  Google Scholar 

  29. Bennett MH, Gallagher MDS, Bestwick CS, Rossiter JT, Mansfield JW: The phytoalexin response of lettuce to challenge by Botrytis cinerea, Bremialactucae and Pseudomonassyringae pv.phaseolicola. Physiol Mol, Plant Pathol. 1994, 44: 321-333. 10.1016/S0885-5765(05)80046-3.

    Article  CAS  Google Scholar 

  30. Ye X-J, Ng T-B, Wu Z-J, Xie L-H, Fang E-F, Wong J-H, Pan W-L, Wing S-S-C, Zhang Y-B: Protein from red cabbage (Brassica oleracea) Seeds with antifungal, antibacterial, and anticancer activities. J Agr Food Chem. 2011, 59: 10232-10238. 10.1021/jf201874j.

    Article  CAS  Google Scholar 

  31. Gonzalex LF, Valedon A, Stiehil WL: Depressant pharmacological effects of component isolated from lettuce, lactuca sativa. Int J Crude Drug Res. 1996, 24: 154-

    Article  Google Scholar 

  32. Sid SA, El-Kashef H, El Mazes , Slam OMM: Phytochemical and pharmacological studies on Lactuca sativa seed oil. Fitoterapia. 1996, 67: 215-219.

    Google Scholar 

  33. Roman RR, Flores S-J, Alarcon AFJ: Anti-hyperglycaemic effect of some edible plants. J Ethnopharmacol. 1995, 48: 25-32. 10.1016/0378-8741(95)01279-M.

    Article  Google Scholar 

  34. Garg M, Garg C, Mukherjee Pulok K, Suresh B: Antioxidant potential of Lactuca sativa. Ancient Sci Life. 2004, 24 (1): 1-4.

    Google Scholar 

  35. Patil RB, Vora SR, Pillai MM: Antioxidant effect of plant extracts on phospholipids levels in oxidatively stressed male reproductive organs in mice. Iran J Rep Med. 2009, 7: 35-39.

    CAS  Google Scholar 

  36. Wambugu SN, Mathiu PM, Gakuya DW, Kanui TI, Kabasa JD, Kiama SG: Medicinal plants used in the management of chronic joint pains in Machakos and Makueni counties, Kenya. J Ethnopharmacol. 2011, 137: 945-955. 10.1016/j.jep.2011.06.038.

    Article  PubMed  Google Scholar 

  37. Michalska K, Stojakowska A, Malarz J, Doležalová I, Lebeda A, Kisiel W: Systematic implications of sesquiterpene lactones in Lactuca species. Biochem Syst Ecol. 2009, 37: 174-179. 10.1016/j.bse.2009.02.001.

    Article  CAS  Google Scholar 

  38. Albone KS, Skin PG: Identification and localization of gibberilins in maturing seed of cucurbit Sechium edule. Planta. 1984, 162: 560-565. 10.1007/BF00399923.

    Article  CAS  PubMed  Google Scholar 

  39. Siciliano T, De Tommasi N, Morelli I, Braca A: Study of flavonoids of Sechium edule (Jacq) swartz (Cucurbitaceae) different edible organs by liquid chromatography photodiode array mass spectrometry. J Agr Food Chem. 2004, 52: 6510-6515. 10.1021/jf040214q.

    Article  CAS  Google Scholar 

  40. Ordonez AAL, Gomez JD, Vattuone MA, Isla MI: Antioxidant activities of Sechium edule (Jacq.) Swartz extracts. Food Chem. 2006, 97: 452-458. 10.1016/j.foodchem.2005.05.024.

    Article  CAS  Google Scholar 

  41. Ordoñez AAL, Gomez JD, Cudmani NM, Vattuone MA, Isla MI: Antimicrobial Activity of Nine Extracts of Sechium edule (Jacq.) Swartz. Microb Ecol Health Dis. 2003, 15: 33-39. 10.1080/0891060010015583.

    Article  Google Scholar 

  42. Gordon EA: The antihypertensive effects of the Jamaican cho-cho. W Indian Med J. 2000, 1: 27-31.

    Google Scholar 

  43. Firdous SM: Protective effect of ethanolic extract and its ethylacetate and n-butanol fractions of Sechium edule fruits against paracetamol induced hepatic injury in mice. Asian J Pharm Clin Res. 2012, 5: 10-14.

    Google Scholar 

  44. Abd Aziz SM, Low CN, Chai LC, Abd Razak SSN, Selamat J, Son R, Sarker MZI, Khatib A: Screening of selected Malaysian plants against several food borne pathogen bacteria. Int Food Res J. 2011, 18: 1195-1201.

    Google Scholar 

  45. Suresh R, Saravanakumar M, Suganyadevi P: Anthocyanins from indian cassava (manihot esculenta crantz) and its antioxidant properties. Int Food Res J. 2011, 18: 1195-1201.

    Google Scholar 

  46. Zakaria ZA, Khairi HM, Somchit MN, Sulaiman MR, Mat Jais AM, Reezal I, Mat Zaid NN, Abdul Wahab SNZ, Fadzil NS, Abdullah M, Fatimah CA: The in vitro antibacterial activity and brine shrimp toxicity of Manihot esculenta var. Sri Pontian extracts. Int J Pharmacol. 2006, 2: 216-220.

    Article  Google Scholar 

  47. The Health Benefits of Green Beans. http://www.elements4health.com/green-beans.html, Accessed on July, 12, 2012

  48. Doss A, Pugualenthi M: Evaluation of antioxydant activity and phytochemical screening of Malus domestica Borkh (apple) and Phaseolus vulgaris L. (green beans). Journal of Pharmaceutical and Scientific Innovation. 2012, 3: 1-4.

    Google Scholar 

  49. Chaurasia S, Saxena R: Antibacterial Activity of Four Different Varieties of Green Beans. Res J Pharm Biol Che Sci. 2012, 3: 70-74.

    Google Scholar 

  50. Sarkar S, Guha D: Effect of ripe fruit pulp extract of Cucurbita pepo Linn. in aspirin induced gastric and duodenal ulcer in rats. Indian J Exp Biol. 2008, 46: 639-645.

    CAS  PubMed  Google Scholar 

  51. Karpagam T, Varalakshmi B, Bai JS, Gomathi S: Effect of different doses of Cucurbita pepo linn extract as an anti-Inflammatory and analgesic nutraceautical agent on inflamed rats. IJPRD. 2011, 3: 184-192.

    Google Scholar 

  52. Carbin BE, Larsson B, Lindahl O: Treatment of benign prostatic hyperplasia with phytosterols. B J Urol. 1990, 66: 639-641. 10.1111/j.1464-410X.1990.tb07199.x.

    Article  CAS  Google Scholar 

  53. Carbin BE, Eliasson R: Treatment by curbicin in benign prostatic hyperplasia (BPH). Swed J Biol Med. 1989, 2: 7-9.

    Google Scholar 

  54. al-Zuhair H, Abd el-Fattah AA, el Latif HA A: Efficacy of Simvastatin and pumpkin-seed oil in the management of dietary-induced hypercholesterolemia. Pharmacol Res. 1997, 3: 403-408.

    Article  Google Scholar 

  55. Nkosi CZ, Opoku AR, Terblanche SE: Effect of pumpkin seed (Cucurbita pepo) protein isolate on the activity levels of certain plasma enzymes in CCl4-induced liver injury in low-protein fed rats. Phytother Res. 2005, 19: 341-345. 10.1002/ptr.1685.

    Article  CAS  PubMed  Google Scholar 

  56. Sharma LD, Bagha HS, Srivastava PS: In vitro anthelmintic screening of indigenous medicinal plants against Haemonchus contortus (Rudolphi, 1803) Cobbold, 1898 of sheep and goats. Indian J Anim Resour. 1971, 5: 33-38.

    Google Scholar 

  57. Adepoju GKA, Adebanjo AA: Effect of consumption of Cucurbita pepo seeds on haematological and biochemical parameters. Afr J Pharm Pharacol. 2011, 5: 18-22.

    Article  Google Scholar 

  58. Jain RAS, Gupta SSPI, Gabrani R: Solanum nigrum: current perspectives on therapeutic properties. Altern Med Rev. 2011, 16: 78-85.

    PubMed  Google Scholar 

  59. Calderón-Montaño JM, Burgos-Morón E, Pérez-Guerrero C, López-Lázaro M: A review on the dietary flavonoid kaempferol. Mini Rev Med Chem. 2011, 11: 298-344. 10.2174/138955711795305335.

    Article  PubMed  Google Scholar 

  60. Marie-Magdeleine C, Udino L, Philibert L, Bocage B, Archimede H: In vitro effects of Cassava (Manihot esculenta) leaf extracts on four development stages of Haemonchus contortus. Vet Parasitol. 2010, 173: 85-92. 10.1016/j.vetpar.2010.06.017.

    Article  CAS  PubMed  Google Scholar 

  61. Cai X, Chin Y, Oh S, Kwon O, Ahn K, Lee H: Anti-inflammatory constituents from Solanum nigrum. B Korean Chem Soc. 2010, 31: 199-201. 10.5012/bkcs.2010.31.01.199.

    Article  CAS  Google Scholar 

  62. Rawani A, Ghosh A, Chandra G: Mosquito larvicidal activities of Solanum nigrum L. leaf extract against Culex quinquefasciatus Say. Parasitol Res. 2010, 107: 1235-1240. 10.1007/s00436-010-1993-9.

    Article  PubMed  Google Scholar 

  63. Kumar S, Bagchi GD, Darokar MP: Antibacterial activity observed in the seeds of some Coprophilous plants. Int J Pharmacogn. 1997, 35: 179-184. 10.1076/phbi.35.3.179.13293.

    Article  Google Scholar 

  64. Ndomo AF, Tapondjou1 AL, Tendonkeng F, F MT: Evaluation des propriétés insecticides des feuilles de Callistemon viminalis (Myrtaceae) contre les adultes d’Acanthoscelidesobtectus (Say) (Coleoptera; Bruchidae). Tropicultura. 2009, 27: 137-143.

    Google Scholar 

  65. N’Guessan K, Kadja B, Zirihi GN, Traoré D, L A-A: Screening phytochimique de quelques plantes médicinales ivoiriennes utilisées en pays Krobou (Agboville, Côte-d’Ivoire). Sciences and Nature. 2009, 6: 1-15.

    Google Scholar 

  66. Howard LR, Talcott ST, Brenes CH, Villalon B: Changes in phytochemical and antioxidant activity of selected pepper cultivars (Capsicum Species) as influenced by maturity. J Agr Food Chem. 2000, 48: 1713-1720. 10.1021/jf990916t.

    Article  CAS  Google Scholar 

  67. Koffi-Nevrya RK, Nangabc KC, Koussémona ZY, Loukoubc GY: Antibacterial activity of two bell pepper extracts: Capsicum annuum L and Capsicum frutescens. Int J Food Prop. 2012, 15: 961-971. 10.1080/10942912.2010.509896.

    Article  Google Scholar 

  68. Dastagir MG, Husaain MM, Masum Billah AHM, Ismail M, Quader A: Phytochemical studies on Capsicum frutescens. IJPSDR. 2012, 3 (5): 1507-1510.

    CAS  Google Scholar 

  69. Bouchelta A, Boughdad A, Blenzar A: Effets biocides des alcaloïdes, des saponines et des flavonoïdes extraits de Capsicum frutescens L. (Solanaceae) sur Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae). Biotechnol Agron Soc Environ. 2005, 9: 259-269.

    CAS  Google Scholar 

  70. Harbone JB: Phytochemical methods: a guide to modern techniques of plant analysis. 1973, London: Chapman & Hall

    Google Scholar 

  71. 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. 10.1055/s-2006-957563.

    Article  CAS  PubMed  Google Scholar 

  72. 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. 10.1016/j.sajb.2005.08.002.

    Article  Google Scholar 

  73. 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: 17-24. 10.1016/j.jep.2008.07.026.

    Article  CAS  PubMed  Google Scholar 

  74. Cohen MA, Huband MD, Yoder SL, Gage JW, Roland GE: Bacterial eradication by clinafloxacin, CI-990, and ciprofloxacin employing MBC test, in-vitro time-kill and in-vivo time-kill studies. J Antimicrob Chemother. 1998, 41: 605-614. 10.1093/jac/41.6.605.

    Article  CAS  PubMed  Google Scholar 

  75. Cowan MM: Plant products as antimicrobial agents. Clin Microbiol Rev. 1999, 12: 564-582.

    CAS  PubMed  PubMed Central  Google Scholar 

  76. Kuete V: Potential of cameroonian plants and derived products against microbial infections: a review. Planta Med. 2010, 76: 1479-1491. 10.1055/s-0030-1250027.

    Article  CAS  PubMed  Google Scholar 

  77. Voukeng IK, Kuete V, Fankam AG, Dzoyem JP, Noumedem JAK, Kuiate J-R, Pages J-M: Antibacterial and antibiotic-potentiation activities af the methanol extract of some Cameroonian spices against Gram-negative multi-drug resistant phenotypes. BMC Res Notes. 2012, 5: 299-10.1186/1756-0500-5-299.

    Article  PubMed  PubMed Central  Google Scholar 

  78. 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: 71-81.

    Google Scholar 

  79. Barkat M, Kadri F: Impact de deux modes de cuisson sur la teneur en polyphénols solubles de six légumes. Revue de génie industriel. 2011, 6: 41-45.

    Google Scholar 

  80. Amarowicz R, Dykes GA, B PR: Antibacterial activity of tannin constituents from Phaseolus vulgaris, Fagoypyrum esculentum, Corylus avellana and Juglans nigra. Fitoterapia. 2008, 79: 217-219. 10.1016/j.fitote.2007.11.019.

    Article  CAS  PubMed  Google Scholar 

  81. Shariati A, Pordeli HR, Khademian A, Aydani M: Evaluation of the antibacterial effects of Capsicum spp. extracts on the Multi-resistant Staphylococcus aureus strains. J Plant Sci Res. 2010, 17: 10-16.

    Google Scholar 

  82. Carbonnelle B, Denis F, Marmonier A, Pinon G, Vague R: Bactériologie médicale: Techniques usuelles. 1987, Paris: SIMEP ed

    Google Scholar 

  83. Mbaveng AT, Ngameni B, Kuete V, Simo KI, Ambassa P, Roy R, Bezabih M, Etoa F-X, Ngajui TB, Abegaz BM, Meyer JJ, Lall N, Beng VP: Antimicrobial activity of the crude extracts and five flavonoids from the twigs of Dorstenia barteri (Maraceae). J Ethnopharmacol. 2008, 116: 483-489. 10.1016/j.jep.2007.12.017.

    Article  CAS  PubMed  Google Scholar 

Pre-publication history

Download references

Acknowledgements

Authors are thankful to Prof. Dumitru Cojocaru (University Alexandru Ioan Cuza, Iasi-Romania), the Romanian Government and The Agence Universitaire de la Francophonie for travel grant to JAKN, and also to Professor Jean-Marie Pages (through VK), Chair of the UMR-MD1 Unit, Université de la Méditerranée, France for providing us with MDR bacteria.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Jules R Kuiate or Victor Kuete.

Additional information

Competing interest

The authors declare that they have no competing interest.

Authors’ contributions

JAKN, MM, STL and MS carried out the study; VK designed the experiments. JAKN, MM and VK wrote the manuscript; VK and JRK supervised the work; VK provided the bacterial strains; all authors read and approved the final manuscript.

Electronic supplementary material

Rights and permissions

Open Access This article is published under license to BioMed Central Ltd. This is an Open Access article is distributed under the terms of the Creative Commons Attribution License ( https://creativecommons.org/licenses/by/2.0 ), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Reprints and permissions

About this article

Cite this article

Noumedem, J.A., Mihasan, M., Lacmata, S.T. et al. Antibacterial activities of the methanol extracts of ten Cameroonian vegetables against Gram-negative multidrug-resistant bacteria. BMC Complement Altern Med 13, 26 (2013). https://doi.org/10.1186/1472-6882-13-26

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/1472-6882-13-26

Keywords