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

BMC Complementary and Alternative MedicineThe official journal of the International Society for Complementary Medicine Research (ISCMR)201313:26

DOI: 10.1186/1472-6882-13-26

Received: 28 September 2012

Accepted: 28 January 2013

Published: 31 January 2013

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.

Keywords

Antibacterial Gram-negative bacteria Multi-drug resistant Extract Vegetable

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

Plant (family); and voucher numbera

Traditional uses

Parts used traditionally

Bioactive or potentially bioactive components

Bioactivities of extracts and/or compounds

Amarantus hybridus Linn (Amarantaceae); 15630 HNC

intestinal bleeding, diarrhoea and excessive menstruation [5, 10]

Leaves, seeds

flavonoids, steroids, terpenoids, cardiac glycosides [5] alkaloid, saponin, tannins, phenols, hydrocyanic acid and phytic acid [11, 12]

antimicrobial [5, 13]

Vernonia calvoana (H.F.) Hook

wounds [14],anticancer [15], fever, stomach ache, diarrhoea, hernia, spleen enlargement [16]

leaves

vernolepin [17, 18], vernomenin [18], flavonoids (quercetin, apigenin, luteolin) [19]

cytotoxic [17], spasmolytic, anti-aggregating and de-aggregating activities, 2 antitumor activity, antimicrobial [20], insecticide [21], antifilarial [22]

(Asteraceae); 42401/HNC

Lactuca sativa Linn; (Asteraceae); 25624/SRF.Cam

analgesic, conjunctivitis, tired eyes, Insomnia, sedative [23] insomnia, anxiety, neurosis, dry coughs, rheumatic pain [24] stimulate digestion, enhance appetite and relieve inflammation [25]

leaves

phenolic acids, triterpenoids, saponins, phytol [23], carotenoids [26], flavonoids including kaempherol [19] Lettucenin-A guaianolide sesquiterpenelactones conjugates, lactucin, deoxylactucin and lactucopicrin [27]

antimicrobial [28], antifungal, antibacterial [29], antitumor [30] antioxidating, analgesic, and anti-inflammatory [23] depressant [31] sedative, hypnotic, analgesic and anticonvulsant [32] hypoglycaemic [33] antioxidant l [34, 35], and anxiolytic

Lactuca capensis Thumb (Asteraceae); 27743 HNC

antispasmodic, digestive, diuretic, hypnotic, narcotic and sedative properties. treatment of insomnia, anxiety, neuroses, hyperactivity in children, dry coughs, whooping cough, rheumatic pain, chronic join pains [36]

leaves

lactucarium, sesquiterpene lactone [37]

 

Sechium edule (Jacq) SW (Cucurbitaceae); 42459/HNC

urine retention, kidney diseases, arteriosclerosis, hypertension [38]

leaves

C-glycosyl and O-glycosyl, flavones in roots, leaves, stem and fruits [39], ascorbic acid,gibberellins, flavonoids and saponins [38]

diuretic [9], free radical-scavenger and antioxydant [40],antibacterial [41], antihypertensive [42] hepatoprotective activity of ethanolic extract and its different [43]

Manihot esculenta Crantz

hypertension, headache and pain, irritable bowel syndrome. fever, headache, aches and pains [44]

leaves

3-rutinosides of kaempferol and quercetin; the cyanogenic glycosides, lotaustralin and linamarin, from the fresh leaves of cassava [45]

anthelmintic activity of crude extracts antibacterial [46]

(Euphorbiaceae); 57650/HNC

leaves

Phaseolus vulgaris Linn (Fabaceae); 42587/HNC

osteoporosis prevention, diuretic, eczema, antiglycemic [47]

cloves

ascorbic acid, phenol, alkaloids, sterols, saponins (aqueous extract), carotenoids like lutein, β-carotene, violanthin and neoxanthin, flavonoids [48] including quercetin, kaemferol, catechins, epicatechins and procyanidins

antioxydant [48], antibacterial [49]

Cucurbita pepo Linn (cucurbitaceae); 15630 HNC

intestinal infections and kidney problems (seeds), minor injuries (flowers), anthelmintic, hypertension, erysipelas, enteritis, dyspepsia, stomach disorders, liver disorders like jaundice [50]

leaves

saponin, tannin, quinone, coumarins, flavonoids, sterol, terpenes, [51] lignin, alkaloids, protein and sugar Curbicin [52] anthocyanin, phenols like syringic acid [52], phytin, lecithin, cucurbitane and hexanocucurbitane L-2-O-β-glucopyranoside, Curbicin [52], flavonoids, Vitamins B, C, and E, β-sitostérol

antihypertensive, anti-oxidative activities,Arthritis, reduce the symptoms of BPH [52, 53]. High Cholesterol, anti-parasitic activity in vi-vitro [54], alleviates the detrimental effects associated with protein malnutrition [55], antiparasitic[56], nephron and hepato-protective, vermifuge, inhibitor of prostaglandin biosynthesis [57], antiparasitic, protects gastric mucosal [50]

Solanum nigrum Linn (Solanaceae); 43000 HNC

pneumonia aching teeth, stomache ache, tonsilitis, tonic,wing worms [14], pain, inflammation and fever. tumor, antioxydant, anti-inflammatory, hepaprotective, diuretic, antipyretic [58]

leaves

kaempferol [19, 59] terpenoids and condensed tannin [60], quercetin, flavonoids [19], polysaccharides, polyphenolic compounds including galic acid, catechin, cafeic acid, rutin and naringenin [58]

anti-inflammatory, antioxidant, anthelmintic activity [60] antinociceptive, antipyretic, antitumor, antiulcerogenic, cancer chemopreventive, hepatoprotective, and immunomodulatory effects [61] Mosquito larvicidal [62], antibacterial [63]

Capsicum frutescens L. (Solanaceae); 10737/SRFcam

wound, male virility [16], insecticide [64], rheumatism, laxative [65] relieve muscle, joint, and toothache pain, to treat cough, asthma, and sore throat, as a stimulant, treat stomach ache, seasickness, and flatulence anciently

fruits

alkaloids, flavonoids, polyphenols [66, 67] and sterols [67] Capsaicin, and dihydrocapsaicin, sterols and polyterpenes, polyphenols, flavonoids, alkaloids, vitamin B2 [65], ortho- hydroxyl- N- benzyl- 16- Methyl-11,14-diene-octadecamide and 9, 12-diene-octadecanoic acid [68], carotenoids, flavonoids and saponins [68, 69]

antibacterial [67], antioxydant [67], insecticidal [69]

a(HNC): Cameroon National Herbarium; (SRFC): Société des Réserves Forestières du Cameroun.

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

Scientific names

Part used

Yield (%)

alkaloids

phenols

tannins

terpènes

stéroids

flavonoids

anthraquinones

anthocyanins

saponins

Amarantus hybridus

leaves

7.9

-

-

-

+

-

+

-

+

-

Vernonia hymenolepis

leaves

9.40

+

+

-

-

-

+

-

-

-

Lactuca sativa

leaves

7.14

+

+

-

-

-

+

-

-

-

Lactuca capensis

leaves

7.14

+

+

+

-

+

-

-

-

-

Sechium edule

leaves

3.76

+

+

-

+

+

+

-

-

+

Manihot esculinta

leaves

07.46

+

+

+

+

+

+

+

-

+

Phaseolus vulgaris

cloves

17.81

+

+

-

-

+

+

-

-

-

Cucurbita pepo

leaves

12.68

+

+

-

-

+

+

-

-

-

solanum nigrum

leaves

11.84

+

+

-

-

+

+

-

-

-

Capsicum frutescens

fruits

16.24

+

+

-

+

-

+

+

-

-

(+): Present; (−): Absent; *The yield was calculated as the ratio of the mass of the obtained methanol extract/mass of the plant powder.

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

Bacteria strains

MIC (μg/ml) of the plant extracts

A. hybridus

V. hymenolepis

L. sativa

L. capensis

S. edule

M. esculenta

P. vulgaris

C. pepo

S. nigrum

C. frutescens

Chloramphenicol1

 

E. coli

ATCC8739

256

1024

512

512

256

256

1024

512

512

512

4

 

ATCC10536

128

256

128

256

128

256

-

256

128

-

4

 

W3110

256

512

256

256

256

512

-

128

256

-

8 (< 2)

 

MC4100

512

1024

512

1024

256

512

1024

256

512

1024

16 (< 2)

 

AG100A

256

512

512

512

256

512

-

512

512

1024

< 2 (< 2)

 

AG100Atet

256

512

512

512

256

512

-

512

512

1024

64 (< 2)

 

AG102

1024

128

1024

512

512

128

-

-

256

512

64 (< 2)

 

AG100

128

1024

128

512

512

512

-

256

128

-

8 (< 2)

 

E. aerogenes

 

ATCC13048

128

1024

256

256

256

256

1024

256

256

-

8

 

EA294

512

512

512

512

512

1024

-

512

512

1024

16

 

CM64

128

128

256

256

128

256

1024

512

256

512

256 (8)

 

EA3

256

256

128

128

256

128

1024

128

128

-

256 (128)

 

EA298

256

512

256

256

256

256

1024

128

256

1024

64 (< 2)

 

EA27

512

128

256

-

512

512

-

512

256

512

≥ 256 (< 2)

 

EA289

-

512

1024

256

512

256

1024

128

1024

256

≥ 256 (64)

 

K. pneumoniae

 

ATCC11296

256

512

256

512

512

512

512

256

256

-

8

 

KP55

256

512

256

512

256

512

1024

256

256

256

32 (4)

 

KP63

256

256

256

256

256

256

-

512

256

512

64 (< 2)

 

K2

512

-

512

512

1024

512

-

1024

512

1024

32 (< 2)

 

K24

512

1024

512

512

512

-

1024

512

512

1024

16 (< 2)

 

P. aeruginosa

 

PA01

256

512

512

256

256

512

-

256

512

-

16

 

PA124

512

1024

512

512

512

512

-

512

512

-

32 (< 2)

 

P. stuartii

 

ATCC29916

128

128

256

1024

128

1024

-

1024

256

-

16

 

NAE16

128

512

256

256

256

256

1024

512

256

-

64 (8)

 

PS2636

512

512

256

256

256

256

-

256

256

512

32

 

PS299645

512

1024

1024

512

512

512

-

512

1024

-

32 (< 2)

 

E. cloacae

 

BM47

128

256

512

1024

256

1024

-

128

512

-

≥ 256 (< 2)

 

ECCI69

256

512

512

256

256

128

-

256

512

-

≥ 256 (16)

 

BM67

256

512

512

256

256

512

1024

128

512

1024

128 (32)

 

The results are shown as average values from three separate experiments.

(−) MIC > 1024 μg/ml.

1 - chloramphenicol was used as a reference antibiotic. MIC was measured in absence and presence of PAßN (in brackets).

Table 4

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

Bacteria strains

A. hybridus

V. hymenolepis

L. sativa

L. capensis

S. edule

M. esculenta

Green bean (P. vulgaris)

C. pepo

S. nigrum

C. frutescens

Chloramphenicol1

E. coli

ATCC8739

-

-

-

-

1024

1024

-

512

-

-

64

ATCC10536

1024

-

-

-

-

-

-

1024

-

-

128

W3110

1024

512

256

-

512

-

-

512

-

-

-

MC4100

1024

-

-

-

-

-

-

-

-

-

-

AG100A

-

1024

512

-

-

512

-

-

-

-

-

AG100Atet

-

1024

512

-

-

-

-

-

-

-

-

AG102

-

-

512

1024

-

-

-

-

-

-

-

AG100

256

1024

-

1024

-

512

-

1024

-

-

-

E. aerogenes

-

-

-

 

-

   

512

  

ATCC13048

   

1024

 

1024

-

1024

 

-

128

EA294

-

-

-

-

-

1024

-

-

-

-

32

CM64

512

-

-

512

512

512

-

-

-

-

-

EA3

1024

512

1024

1024

-

512

-

1024

1024

-

-

EA298

512

1024

1024

-

1024

256

-

256

512

-

-

EA27

-

-

-

-

-

512

-

-

-

-

-

EA289

-

1024

-

512

1024

512

-

-

-

-

-

K. pneumoniae-

ATCC11296

-

-

-

1024

-

-

-

256

1024

-

64

KP55

1024

-

-

-

1024

1024

-

1024

512

-

128

KP63

512

512

-

-

-

-

-

512

1024

-

-

K2

1024

-

-

1024

-

-

-

-

-

-

256

K24

-

-

-

-

1024

-

-

512

-

-

512

P. aeruginosa

PA01

-

-

-

-

-

-

-

-

-

-

256

PA124

-

1024

-

1024

-

-

-

1024

512

-

-

P. stuartii

ATCC29916

-

256

-

1024

1024

1024

-

1024

512

-

128

NAE16

-

-

512

-

1024

-

-

1024

-

-

256

PS2636

512

 

1024

1024

-

1024

-

512

-

-

-

PS299645

-

-

-

-

-

-

-

-

-

-

-

E. cloacae

BM47

-

1024

512

-

-

-

-

-

1024

-

-

ECCI69

1024

512

-

1024

512

1024

-

1024

512

-

-

BM67

512

1024

-

1024

1024

1024

-

1024

-

-

-

The results are shown as average values from three separate experiments.

(−) MBC > 1024 μg/ml.

1 - chloramphenicol was used as a reference antibiotic.

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.

Declarations

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.

Authors’ Affiliations

(1)
Department of Biochemistry, Faculty of Science, University of Dschang
(2)
Department of Biochemistry and Molecular Biology, Faculty of Biology, Alexandru Ioan Cuza University

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, 2012Google 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: FormatexGoogle 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.View ArticlePubMedPubMed CentralGoogle 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.View ArticleGoogle 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 LimitedGoogle 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.View ArticleGoogle 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.View ArticleGoogle 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.View ArticleGoogle 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 PublishingGoogle 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.View ArticleGoogle Scholar
  18. Sims RJ: Synthesis of furanosesquiterpenoid natural products. 1981, Southampton: University Of SouthamptonGoogle 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.PubMedGoogle 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 BamakoGoogle 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.View ArticleGoogle Scholar
  24. Katz SH, Weaver WW: Encyclopidia of food and culture. 2003, New York: In. schribner EdGoogle 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.View ArticlePubMedGoogle 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.View ArticlePubMedGoogle 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.View ArticleGoogle 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.PubMedGoogle 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.View ArticleGoogle 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.View ArticleGoogle 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-View ArticleGoogle 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.View ArticleGoogle 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.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.View ArticlePubMedGoogle 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.View ArticleGoogle 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.View ArticlePubMedGoogle 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.View ArticleGoogle 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.View ArticleGoogle 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.View ArticleGoogle 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.View ArticleGoogle 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.PubMedGoogle 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.View ArticleGoogle 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.View ArticleGoogle 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.View ArticlePubMedGoogle 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.View ArticleGoogle Scholar
  58. Jain RAS, Gupta SSPI, Gabrani R: Solanum nigrum: current perspectives on therapeutic properties. Altern Med Rev. 2011, 16: 78-85.PubMedGoogle 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.View ArticlePubMedGoogle 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.View ArticlePubMedGoogle 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.View ArticleGoogle 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.View ArticlePubMedGoogle 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.View ArticleGoogle 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.View ArticleGoogle 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.View ArticleGoogle Scholar
  68. Dastagir MG, Husaain MM, Masum Billah AHM, Ismail M, Quader A: Phytochemical studies on Capsicum frutescens. IJPSDR. 2012, 3 (5): 1507-1510.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.Google Scholar
  70. Harbone JB: Phytochemical methods: a guide to modern techniques of plant analysis. 1973, London: Chapman & HallGoogle 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.View ArticlePubMedGoogle 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.View ArticleGoogle 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.View ArticlePubMedGoogle 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.View ArticlePubMedGoogle Scholar
  75. Cowan MM: Plant products as antimicrobial agents. Clin Microbiol Rev. 1999, 12: 564-582.PubMedPubMed CentralGoogle 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.View ArticlePubMedGoogle 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.View ArticlePubMedPubMed CentralGoogle 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.View ArticlePubMedGoogle 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 edGoogle 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.View ArticlePubMedGoogle Scholar
  84. Pre-publication history

    1. The pre-publication history for this paper can be accessed here:http://www.biomedcentral.com/1472-6882/13/26/prepub

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