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Antibacterial and Antibiotic-Potentiating Activities of Thirteen Cameroonian Edible Plants against Gram-Negative Resistant Phenotypes.

1. Introduction

The advent of antibiotics has been a tremendous therapeutic progress as it has significantly reduced mortality due to bacterial infections [1]. However, their misuse in humans and animals has contributed to the emergence of drug-resistant bacteria [2]. These bacteria are often more difficult to be combatted, and the infections they caused are more difficult and expensive to be treated. This can therefore lead to serious disability and even death [3, 4]. According to World Health Organization [4], antibiotic resistance has drastically increased to high levels all over the world. The multidrug-resistant (MDR) genes may be carried on the bacterial chromosome, plasmid, or transposons, and their expression allows bacteria to overcome the effects of many antibiotics [5]. Among the antibiotic resistance mechanisms, the most common are enzymatic inactivation of antibiotics, changes in cell permeability, and induction/activation of efflux pumps [6]. The Gram-negative bacteria are among the bacteria that drastically impair the efficacy of antibacterial agents and therefore limit their clinical use [3, 7]. In fact, to guide research, discovery, and development of new antibiotics against MDR bacteria, WHO has developed a global priority list of antibiotic-resistant bacteria where Gram-negative multidrug-resistant (MDR) bacteria, particularly Pseudomonas aeruginosa and Enterobacteriaceae, constitute the most critical group [4]. These groups of bacteria are particularly characterized by the expression of efflux pumps belonging to the Resistance Nodulation-cell Division (RND) family, which constitutes one of their main resistance mechanisms [8,9]. Tackling antibiotic resistance mechanisms like efflux pumps expression is therefore a high priority for WHO and scientists over the world. Plant sources used since ancient time to fight microbial infections appear as an interesting alternative for the discovery of new antibacterial substances against MDR bacteria [10-12]. For instance, a number of plant-deriving compounds with possible efflux pump inhibitor (EPI) activities such as reserpine [13], berberine [13, 14], and curcumin [15] have been discovered, but they are still unused clinically. In our previous studies, we have also shown that edible plants could be used alone and/or in combination with commonly used antibiotics to fight infections involving Gram-negative MDR bacteria [1619]. In the continuous search for natural substances effective in MDR bacteria, this study was aimed at investigating the in vitro antibacterial and antibiotic-potentiating activities of methanol extracts of thirteen Cameroonian edible plants (Azadirachta indica A. Juss, Citrus grandis (L.) (Red), Citrus grandis (L.) (White), Cucurbita maxima Duch., Dacryodes edulis [G. Don] H. J. Lam, Hibiscus esculentus L., Ipomoea batatas (L.) Lam., Irvingia gabonensis (Aubry. Lec. ex O. Rorke) Baill., Phaseolus vulgaris L., Saccharum officinarum L., Spondias mombin L., Theobroma cacao L., and Uapaca guineensis Muell. Arg.) against Gram-negative MDR phenotypes. Some of these plants or their related genera are known for their antimicrobial properties, but not as antibiotic modulators (Supplementary Materials, Table S1).

2. Material and Methods

2.1. Plant Material and Extraction. Plants used in this study were collected in West, Southwest, and Centre regions of Cameroon from March to April 2016. All plants collected were identified at the National Herbarium (Yaounde, Cameroun) where the voucher specimens were deposited. The names as well as the reference numbers of the studied plants are shown in Table S1 (Supplementary Materials). For the extraction, each plant material was cleaned and air-dried, and the powder (200 g) was soaked in methanol (MeOH, 1 L) for 48 h at room temperature. The extract obtained was collected by filtration using Whatman filter paper n[degrees].1 and concentrated under reduced pressure using a rotary evaporator to yield a residue which constituted the plant extract. All the extracts were then kept at 4[degrees] C until further use.

2.2. Preliminary Phytochemical Investigations. The major phytochemical classes such as triterpenes (Liebermann-Burchard test), sterols (Salkowski's test), alkaloids (Mayer's test), polyphenols (ferric chloride test), flavonoids (aluminum chloride test), anthraquinones (Borntrager's test), saponins (foam test), and tannins (gelatin test) were investigated as previously described [20, 21].

2.3. Chemicals for Antibacterial Assays. Eight reference antibiotics were used in this study: ampicillin (AMP), cefepime (CEF), chloramphenicol (CHL), ciprofloxacin (CIP), erythromycin (ERY), kanamycin (KAN), streptomycin (STP), and tetracycline (TET) which were obtained from Sigma-Aldrich, St Quentin Fallavier, France. p-Iodonitrotetrazolium (INT) (Sigma-Aldrich) chloride was used as microbial growth indicator; dimethylsulfoxide (DMSO) was used to dissolve the plant extracts [22].

2.4. Bacteria Strains and Culture Media. In this study, we used a panel of 21 strains belonging to Gram-negative bacteria including sensitive and multidrug-resistant strains of Escherichia coli, Enterobacter aerogenes, Enterobacter cloacae, Klebsiella pneumoniae, Providencia stuartii, and Pseudomonas aeruginosa. Their features were previously reported (Supplementary Materials, Table S2). These bacteria were maintained at 4[degrees]C and subcultured on a fresh Mueller Hinton Agar (MHA) for 24 h before any antibacterial assay. Mueller Hinton Broth (MHB) was used for antibacterial assays [23].

2.5. Antibacterial Assays. MIC and MBC values of the different samples were determined by microdilution using INT colorimetric assay as previously described [22, 24]. Briefly, the samples were dissolved in 10% dimethyl-sulfoxide (DMSO)/Mueller Hinton Broth (MHB) and serially diluted twofold (in a 96-well microplate). Then, 100 [micro]L of inoculum (2 x [10.sup.6] CFU/mL) prepared in MHB was added in each well. Chloramphenicol was used as reference drug and the well containing the vehicle (DMSO 2.5%) as control. The plates were then covered with a sterile plate sealer and gently shaked to mix the contents of the wells. After 18 h of incubation at 37[degrees]C, the MIC value of each sample, defined as the lowest sample concentration that inhibited complete bacteria growth, was detected following addition of 40 [micro]L INT (0.2 mg/mL) and incubation at 37[degrees]C for 30 min. Viable bacteria reduced the yellow dye to pink. The MBC value was determined by adding 50 [micro]L aliquots of the preparations, which did not show any growth after incubation during MIC assays, to 150 [micro]L of MHB. Then, these preparations were incubated at 37[degrees]C for 48 h. The MBC was regarded as the lowest concentration of samples, which did not produce a color change after addition of INT as mentioned above [24]. Each assay was performed in three independent tests in triplicate. In case there was difference, the MIC or MBC values were taken as the most frequently occurring values.

2.6. Antibiotic Resistance Modifying Assay. The resistance modifying activity of the extracts was evaluated by determining the MICs of antibiotics in the presence or absence of the plant extracts in the 96-wells modulation assay as previously described [13, 25]. Briefly, after serial dilutions of antibiotics (256-0.5 [micro]g/mL), the plant extracts were added at their subinhibitory concentrations (MIC/2 and MIC/4) selected after preliminary study assessed against P. aeruginosa PA124 (Supplementary Materials, Table S3). The MIC of each treatment was determined as described above. Each assay was performed in three independent tests in duplicate. Modulation factors (MF), calculated as MIC of antibiotic alone/MIC of antibiotic + extract, were used to express the antibiotic-potentiating effects of the plant extracts [11, 26, 27].

3. Results

3.1. Qualitative Phytochemical Composition of the Tested Extracts. The results of the phytochemical screening (Table 1) showed that only Theobroma cacao broad bean (TCBB) extract contained all the classes of screened secondary metabolites. These metabolites were selectively distributed in other tested plant extracts. In addition, results showed that polyphenols, tannins, triterpenes, and steroids were the most represented metabolites in the tested extracts.

3.2. Antibacterial Activity of the Tested Extracts. Nineteen extracts from thirteen plants as well as chloramphenicol were tested for their antibacterial activities on a panel of 21 Gram-negative bacteria. The results of Table 2 show that the tested extracts (A. indica bark, P. vulgaris leaves, H. esculentus leaves, U. guineensis leaves, and D. edulis seed) presented selective antibacterial activity with the recorded MIC values ranging from 64 to 1024 [micro]g/mL. Some extracts presented broad spectrum of antibacterial activity. Their inhibitory activities were observed on 18/21 (85,71%, A. indica bark and P. vulgaris leaves), 17/21 (80.95%, H. esculentus leaves), and 16/21 (76, 19%, U. guineensis leaves and D. edulis seeds). The lowest MIC value (64 [micro]g/mL) was recorded with the extract of T. cacao broad bean (TCBB) against E. coli ATCC 8739, AG100ATet, and K. pneumoniae K24 and that from bark of U. guineensis against E. coli ATCC 8739. In general, MBC values were not detected at up to 1024 [micro]g/mL extract concentrations. Extract from I. batatas leaves (IBL) and T. cacao leaves (TCL) displayed the best MBC values (256 [micro]g/mL) against E. aerogenes EA27.

3.3. Antibiotic Resistance-Modifying Activities of the Extracts. The antibacterial activity of 6 commonly used antibiotics was evaluated in the presence of plant extracts at the concentrations equivalent to MIC/2 and MIC/4. The results obtained are summarized in Tables 3-9. From these tables, it was observed that some extracts selectively improved the antibacterial activities of tested antibiotics against the selected MDR bacteria (2- to 64-fold decrease of MIC). D. edulis seeds extract has significantly improved the antibacterial activities of CHL and KAN against 90% (8/10) and 80% (8/10) of the tested MDR bacteria, respectively (Table 4). The bark extract of A. indica (Table 3) and leaves extract of P. vulgaris (Table 6) also improved the activities of CHL, STP, and TET to about 80% (8/10) and 70% (7/10) of the tested MDR bacteria, respectively. The modulating effects were also observed after the combination of T. cacao leaves extract with STP, CHL, CIP, TET, and STP against 80% to 70% of the tested MDR bacteria (Table 8) whilst other extracts were less active.

4. Discussion

Plants constitute an undeniable source of substances named secondary metabolites which are known for their direct or indirect antimicrobial activities; some examples include flavonoids, phenols, terpenoids and sterols, saponins, and tannins [28-30]. The results of the phytochemical screening carried out on the tested extracts indicated the presence of at least one of these metabolites in each of the tested extracts (Table 1). This may explain the antibacterial activities of the extracts tested.

According to Tamokou et al. [31], an edible plant extract is very active if it has a MIC<100 [micro]g/mL, significantly active if 100 < MIC<512 [micro]g/mL, moderately active when 512<MIC [less than or equal to] 2048 [micro]g/mL, and weakly active for a MIC>2048 [micro]g/mL. Thus, many of the tested extracts presented significant to moderate activities, 100< MIC<2048 [micro]g/mL. Therefore, two extracts were very active (MIC<100 [micro]g/mL), including the extract from seeds of Theobroma cacao, active against E. coli ATCC8739, AG100Atet, and K. pneumoniae K 24 and the extract from bark of Uapaca guineensis which was very active on E. coli ATCC 8739 (Table 2). Several other studies have already demonstrated the in vitro antibacterial activity of at least one of the parts of these two plants or those belonging to the same genus. Previous study has already demonstrated the antibacterial potential of extracts of bark and pulp of T. cacao on many bacterial strains including E. coli [32]. Singh et al. [33] have also demonstrated the antibacterial activity of T. cacao seed extract against K. pneumoniae. In addition, the bark of several species of the Uapaca genus has shown very good antibacterial activity against certain sensitive and resistant strains [34, 35]; the results obtained in this work reinforce those previous works done with some of the tested extracts. The extracts of seeds of Theobroma cacao and that from bark of Uapaca guineensis could be used to fight infections involving multidrug-resistant bacteria.

In addition to their direct antibacterial activities, secondary metabolites have been found to act indirectly as modulators of the activity of antibacterial agents [10, 28, 36]. In this work, some antibiotics (CHL, TET, KAN, STR, and ERY) activities were improved (2 to 64 times) on more than 70% of the multidrug-resistant bacteria tested in the presence of T. cacao leaves, P. vulgaris leaves, D. edulis seeds, and A. indica barks extracts (Tables 3-9). The bacteria used in this work are multiresistant and overexpress efflux pumps as a resistance mechanism (Supplementary Materials, Table S2). This suggests that aforesaid extracts could contain substances which are able to inhibit the efflux pumps expressed in these bacteria [37], thus leading to an increase in the effectiveness of antibiotics [38]. Several studies have shown that polyphenols, especially flavonoids, could improve the activity of antibiotics against resistant bacterial strains [39, 40]. Thus, the presence of these metabolites in the most active extracts may be the origin of the observed antibiotic-potentiating activity. Many cases of antagonism were also observed and this could be due to the negative interactions between the antibiotics and the compounds of the plant extract, leading, for example, to the inhibition of the active groups of the antibiotics. These results of this study indicate, for the first time, the potential of the tested plant extracts, mainly extracts from D. edulis, P. vulgaris, A. indica, and T. cacao, to reverse antibiotic resistance.

5. Conclusion

This work has provided informative data related to the antimicrobial activity of the tested plant extracts. It suggests that plant extracts and particularly those from Theobroma cacao and P. vulgaris can be used alone or in combination with conventional antibiotics in the treatment of bacterial infections involving multiresistant phenotypes.

Data Availability

The data used to support the findings of this study are included within the article.

https://doi.org/10.1155/2018/4020294

Conflicts of Interest

The authors declare that there are no conflicts of interest regarding the publication of this paper.

Authors' Contributions

Brice E. N. Wamba, Paul Nayim, Aime G. Fankam, and Joachim K. Dzotam carried out the study; Armelle T. Mbaveng and Victor Kuete designed the experiments. Aimee G. Fankam and Victor Kuete wrote the manuscript; Armelle T. Mbaveng and Victor Kuete supervised the work and provided the facilities for antibacterial assays; all authors read and approved the final manuscript.

Acknowledgments

The authors are thankful to the Cameroon National Herbarium for identification of plants.

Supplementary Materials

Supplementary file.docx. Table S1: information on the studied plants; Table S2: further details on the antibiotic resistance profiles of tested Gram-negative bacteria; Table S3: results of preliminary evaluation of antibiotic resistance modulatory activity of selected extracts at subinhibitory concentrations against Pseudomonas aeruginosa PA124. (Supplementary Materials)

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Paul Nayim, Armelle T. Mbaveng (iD), Brice E. N. Wamba, Aime G. Fankam, Joachim K. Dzotam, and Victor Kuete (iD)

Department of Biochemistry, Faculty of Science, University of Dschang, Cameroon

Correspondence should be addressed to Armelle T. Mbaveng; armbatsa@yahoo.fr and Victor Kuete; kuetevictor@yahoo.fr

Received 24 March 2018; Revised 24 June 2018; Accepted 17 July 2018; Published 10 September 2018

Academic Editor: Slim TOUNSI
Table 1: Extraction yields and phytochemical composition
of the plant extracts.

Plant extract             Part used   Yields (%)   ALK   POL   FLAY

Azadirachta indica          Bark         10.3       +     +     -
Citrus grandis (Red)      Pericarp       13.4       +     +     +
                           Leaves        6.2        -     -     -
Citrus grandis (White)     Leaves        2.6        +     +     -
Cucurbita maxima            Beans        2.6        -     +     -
                           Leaves        6.2        -     +     +
Dacryodes edulis            Bark         9.1        -     +     -
                            Seeds        6.9        -     +     +
Hibiscus esculentus        Leaves        1.9        -     +     -
Ipomoea batatas             Beans        3.3        +     +     +
Irvingia gabonensis        Leaves        6.7        -     +     -
Phaseolus vulgaris         Leaves        1.2        -     +     -
Spondias mombin            Leaves        21.4       -     +     -
Saccharum officinarum      Leaves        8.4        -     +     -
Theobroma cacao            Leaves        3.1        -     +     -
                            Beans        6.2        +     +     +
Uapaca guineensis          Leaves        7.3        -     +     -
                            Bark         6.1        +     +     -

Plant extract             Part used   ANTHR   TAN   TRI   STER   SAP

Azadirachta indica          Bark        -      +     -     +      +
Citrus grandis (Red)      Pericarp      -      +     +     +      -
                           Leaves       -      -     +     +      -
Citrus grandis (White)     Leaves       -      +     +     +      -
Cucurbita maxima            Beans       -      +     +     +      +
                           Leaves       +      +     +     +      +
Dacryodes edulis            Bark        +      +     +     +      +
                            Seeds       +      +     +     +      +
Hibiscus esculentus        Leaves       -      +     -     +      -
Ipomoea batatas             Beans       +      +     +     -      +
Irvingia gabonensis        Leaves       -      +     -     +      +
Phaseolus vulgaris         Leaves       -      +     -     +      +
Spondias mombin            Leaves       -      +     +     +      -
Saccharum officinarum      Leaves       -      +     -     +      +
Theobroma cacao            Leaves       -      +     +     +      +
                            Beans       +      +     +     +      +
Uapaca guineensis          Leaves       -      +     +     +      +
                            Bark        -      +     +     +      +

(-): absent; (+): present; yield calculated as the ratio of the
mass of the obtained methanol extract/mass of the plant powder;
ALK: alkaloids; ANTH: anthocyanins; ANTHR: anthraquinones; FLAV:
flavonoids; POL: polyphenols; SAP: saponins; STER: steroids;
TAN: tannins; TRI: triterpenes.

Table 2: MIC and MBC of the plant extracts and chloramphenicol
against bacteria strain.

    Samples (b) MIC and MBC in [micro]g/ml. (in Bracket)

Bacterial
strains (a)         AIB         CGrP       CGrL        CGwL

E. coli
  ATTC8739        1024 (-)    1024 (-)   1024 (-)    1024 (-)
  ATCC10536       1024 (-)    1024 (-)   1024 (-)       --
  AG100           1024 (-)       --      1024 (-)    512 (-)
  AG102           1024 (-)       --       512 (-)       --
  AG100Atet       1024 (-)    1024 (-)    256 (-)    512 (-)
  MC4100          1024 (-)       --       256 (-)       --
  W3110           1024 (-)       --      1024 (-)       --
E. aerogenes
  ATCC13048       1024 (-)       --         --          --
  EA27           512 (1024)      --         --       1024 (-)
  EA289           1024 (-)       --      1024 (-)     128(-)
  EA294           1024 (-)       --      1024 (-)       --
  EA 298          512 (-)     1024 (-)      --       1024 (-)
K. pneumoniae
  ATCC11296          --       1024 (-)   1024 (-)     128(-)
  K24             1024 (-)       --      128 (512)      --
  KP55            1024 (-)       --         --          --
  KP63           512 (1024)      --         --          --
P. stuartii
  PS2636             --          --         --          --
  NEA16              --          --         --          --
E. cloacae
  ECCI69          512 (-)     1024 (-)      --          --
P. aeruginosa
  PA01            1024 (-)       --      1024 (-)       --
  PA124           1024 (-)    1024(-)     512 (-)    512 (-)

     Samples (b) MIC and MBC in [micro]g/ml. (in Bracket)

Bacterial
strains (a)         CMB         DEB         DEL          DES

E. coli
  ATTC8739        1024 (-)       --          --        1024 (-)
  ATCC10536       1024 (-)       --          --           --
  AG100           1024 (-)       --       1024 (-)        --
  AG102           1024 (-)       --          --           --
  AG100Atet          --          --       1024 (-)        --
  MC4100         128 (1024)      --       1024 (-)     1024 (-)
  W3110              --       1024 (-)       --        1024 (-)
E. aerogenes
  ATCC13048          --       1024 (-)    512 (-)      512 (-)
  EA27               --       1024 (-)   512 (1024)    1024 (-)
  EA289           512 (-)     512 (-)    256 (1024)    512 (-)
  EA294              --       1024 (-)    512 (-)     128 (512)
  EA 298             --          --          --        1024 (-)
K. pneumoniae
  ATCC11296          --          --          --        1024 (-)
  K24                --       1024 (-)    512 (-)         --
  KP55           128 (1024)      --          --        1024 (-)
  KP63               --       1024 (-)       --        512 (-)
P. stuartii
  PS2636             --       512 (-)     512 (-)      512 (-)
  NEA16              --       512 (-)     512 (-)      256 (-)
E. cloacae
  ECCI69             --       128 (-)    256 (1024)    128 (-)
P. aeruginosa
  PA01               --       512 (-)     1024 (-)    512 (1024)
  PA124              --          --          --        1024 (-)

    Samples (b) MIC and MBC in [micro]g/ml. (in Bracket)

                    Plant extracts
Bacterial
strains (a)         HEL          IBL        IGB         PVL

E. coli
  ATTC8739        512 (-)     1024 (-)       --       512 (-)
  ATCC10536       1024 (-)       --          --       512 (-)
  AG100           512 (-)        --       1024 (-)   512 (1024)
  AG102           1024 (-)       --          --       512 (-)
  AG100Atet       1024 (-)    1024 (-)       --          --
  MC4100          512 (-)        --          --      256 (512)
  W3110          512 (1024)      --          --       1024 (-)
E. aerogenes
  ATCC13048       256 (-)      256 (-)       --       1024 (-)
  EA27           512 (1024)   256 (256)      --      512 (1024)
  EA289           512 (-)     1024 (-)       --       1024 (-)
  EA294              --          --          --       512 (-)
  EA 298          256 (-)      512 (-)       --       1024 (-)
K. pneumoniae                                --
  ATCC11296       512 (-)      512 (-)    1024 (-)    512 (-)
  K24             512 (-)        --          --       512 (-)
  KP55            512 (-)      512 (-)       --          --
  KP63               --        256 (-)       --       512 (-)
P. stuartii
  PS2636         512 (1024)      --          --       512 (-)
  NEA16           512 (-)        --          --          --
E. cloacae
  ECCI69             --        512 (-)       --       512 (-)
P. aeruginosa
  PA01               --          --          --      512 (1024)
  PA124            512(-)     1024 (-)       --       512 (-)

   Samples (b) MIC and MBC in [micro]g/ml. (in Bracket)

Bacterial
strains (a)        SML        SOL        TCBB        TCL

E. coli
  ATTC8739          --      1024 (-)    64(-)     1024 (-)
  ATCC10536         --         --         --         --
  AG100             --      1024 (-)   1024 (-)      --
  AG102             --      512 (-)    256 (-)       --
  AG100Atet         --         --       64(-)     1024 (-)
  MC4100            --      1024 (-)      --         --
  W3110             --      1024 (-)      --         --
E. aerogenes
  ATCC13048         --      512 (-)       --       256 (-)
  EA27              --      512 (-)    256 (-)    256 (256)
  EA289          1024 (-)   1024 (-)   1024 (-)   1024 (-)
  EA294             --         --         --         --
  EA 298         1024 (-)   512 (-)       --       512 (-)
K. pneumoniae
  ATCC11296         --         --         --       512 (-)
  K24               --      1024 (-)    64(-)        --
  KP55           1024 (-)   512 (-)    1024 (-)    512 (-)
  KP63              --         --      1024 (-)    256 (-)
P. stuartii
  PS2636            --         --         --         --
  NEA16             --      1024 (-)      --         --
E. cloacae
  ECCI69            --         --      1024 (-)    512 (-)
P. aeruginosa
  PA01              --      1024 (-)   1024 (-)      --
  PA124             --      1024 (-)      --         --

Samples (b) MIC and MBC in [micro]g/ml. (in Bracket)

Bacterial                                 Antibiotic
strains (a)         UGB          UGL         CHL

E. coli
  ATTC8739       64 (1024)   256 (1024)     8 (64)
  ATCC10536       128 (-)     1024 (-)      4(16)
  AG100           512 (-)      512 (-)     32 (64)
  AG102          256 (1024)      --        32 (256)
  AG100Atet       256 (-)      512 (-)      4 (32)
  MC4100             --        512 (-)     128 (-)
  W3110              --        512 (-)      8 (32)
E. aerogenes
  ATCC13048          --        512 (-)     8 (128)
  EA27            1024 (-)    1024 (-)    128 (256)
  EA289              --          --         4 (64)
  EA294              --        512 (-)     2 (256)
  EA 298          1024 (-)    1024 (-)     8 (128)
K. pneumoniae
  ATCC11296          --       1024 (-)     8 (256)
  K24             128 (-)      512 (-)     16 (128)
  KP55            512 (-)     1024 (-)     64 (128)
  KP63               --          --        16 (128)
P. stuartii
  PS2636             --       1024 (-)     64 (256)
  NEA16              --       1024 (-)     64 (128)
E. cloacae
  ECCI69             --        512 (-)     128 (-)
P. aeruginosa
  PA01            128 (-)        --        128 (-)
  PA124           512 (-)        --         32 (-)

(a) Bacterial strain [E.c: Escherichia coli, E.a: Enterobacter
aerogenes, K.p: Klebsiella pneumoniae, P.s: Providencia stuartii,
E.cl: Enterobacter cloacae, P.a: Pseudomonas aeruginosa], (b) Samples
[AIB: Azadirachta indica bark, CGrP: Citrus grandis (red) pericarp,
CGrL: Citrus grandis (red) leaves, CGwL: Citrus grandis (white)
leaves, CMB: Cucurbita maxima beans, DEB: Dacryodes edulis bark,
DEL: Dacryodes edulis leaves, DES: Dacryodes edulis seeds, HEL:
Hibiscus esculentus leaves, IBL: Ipomoea batatas leaves, IGB:
Irvingia gabonensis beans, PVL: Phaseolus vulgaris leaves, SML:
Spondias mombin leaves, SOL: Saccharum officinarum leaves, TCBB:
Theobroma cacao beans, TCL: Theobroma cacao leaves, UGB:
Uapacaguineensis bark, UGL: Uapacaguineensis leaves, CHL:
chloramphenicol]. MIC: minimal inhibitory concentration,
MBC: minimal bactericidal concentration, -: MIC and MBC
at up to 1024 [micro]g/mL; MIC in bold: significant activity.

Table 3: Antibiotic resistance modulatory activity of
leaves extract of Azadirachta indica.

                             Bacteria MIC ([micro]g/mL) and modulating
                                        factors (in bracket)

                                     E. coli           E. aerogenes
                 Extract
Antibiotics    concentration    AG102    AG100Atet    EA27      EA289

CHL                  0           64          8         64        64
                  CM 1/2       16 (4)#     8 (1)     32 (2)#   64 (1)
                  CM 1/4       32 (2)#     8 (1)     32 (2)#   64 (1)
KAN                  0           32          4         16        32
                  CM 1/2       16 (2)#     4 (1)     16 (1)    32 (1)
                  CM 1/4       16 (2)#     4 (1)     16 (1)    32 (1)
STP                  0           128        256        256       64
                   CMI/2       128 (1)    256 (1)    256 (1)   32 (2)#
                   CMI/4       128 (1)    256 (1)    256 (1)   64 (1)
CIP                  0            8          1          1         1
                   CMI/2        8 (1)      1 (1)      1 (1)     1 (1)

                   CMI/4        8 (1)      2 (1)      1 (1)     1 (1)
TET                  0            8        < 0.5       64        32
                   CMI/2       1 (8)#    < 0.5(na)   64 (1)    8 (4)#
                   CMI/4       4 (2)#    < 0.5(na)   64 (1)     8 (4)
ERY                  0           64          8         16        64
                   CMI/2       32 (2)#    2 (4)#     16 (1)    32 (2)#
                   CMI/4       32 (2)#    4 (2)#     16 (1)    64 (1)

                             Bacteria MIC ([micro]g/mL) and modulating
                                        factors (in bracket)

                                    K. pneumoniae        P. stuartii
                 Extract
Antibiotics    concentration       KP55         KP 63     PS2636

CHL                  0              64           64         32
                  CM 1/2          8 (8)#       32 (2)#   1 (16)#
                  CM 1/4          64 (1)       32 (2)#    4 (8)#
KAN                  0              64           64         16
                  CM 1/2          64 (1)       64 (1)     16 (1)
                  CM 1/4          64 (1)#      64 (1)     16 (1)
STP                  0              64           256       256
                   CMI/2          8 (8)#       32 (8)#   128 (2)#
                   CMI/4          128 (2)      32 (8)#   256 (1)
CIP                  0               8            4         16
                   CMI/2      <0.5([greater     4 (1)     16 (1)
                              than or equal
                                 to] 16)#
                   CMI/4          16 (1)        4 (1)     16 (1)
TET                  0              16           32         4
                   CMI/2          2 (8)#       16 (2)#    1 (4)#
                   CMI/4          4 (4)#       16 (2)#    1 (4)#
ERY                  0              64           32         16
                   CMI/2          4 (32)#      32 (1)     2 (8)#
                   CMI/4          32 (2)#      32 (1)     4 (4)#

                                 Bacteria MIC ([micro]g/mL) and
                                 modulating factors (in bracket)

                                  P. stuartii       P.aeruginosa
                 Extract
Antibiotics    concentration     NEA16      PA01      PA124

CHL                  0            64         64        32
                  CM 1/2        16 (4)#    32 (2)#   8 (4)#
                  CM 1/4        32 (2)#    32 (2)#   8 (4)#
KAN                  0            32         16        64
                  CM 1/2        4 (4)#     4 (4)#    16 (4)#
                  CM 1/4        4 (8)#     16 (1)    32 (2)#
STP                  0            16         256       64
                   CMI/2        16 (1)     256 (1)   32 (2)#
                   CMI/4        32 (2)     256 (1)   32 (2)#
CIP                  0             2          2        16
                   CMI/2       <0.5(>4)#   1 (2)#    8 (2)#

                   CMI/4         2 (1)      2 (1)    16 (1)
TET                  0            32         16        16
                   CMI/2        16 (2)     2 (8)#    2 (8)#
                   CMI/4        32 (1)     2 (8)#    2 (8)#
ERY                  0            32         16        32
                   CMI/2        32 (1)     8 (2)#    16 (4)#
                   CMI/4        32 (1)     16 (1)    32 (1)

                              Bacteria MIC
                              ([micro]g/mL)
                             and modulating
                               factors
                              (in bracket)

                             P.aeruginosa

                 Extract      Modulating
Antibiotics    concentration   effect (%)

CHL                  0
                  CM 1/2         80.00#
                  CM 1/4         70.00#
KAN                  0
                  CM 1/2         40.00
                  CM 1/4         40.00
STP                  0
                   CMI/2         50.00
                   CMI/4         20.00
CIP                  0
                   CMI/2         20.00

                   CMI/4         00.00
TET                  0
                   CMI/2         80.00#
                   CMI/4         70.00#
ERY                  0
                   CMI/2         70.00#
                   CMI/4         40.00

CHL: chloramphenicol, KAN: kanamycin, STP: streptomycin, CIP:
ciprofloxacin, TET: tetracycline, ERY: erythromycin; -: MIC
not detected at up to 256 [micro]g/mL; ( ): modulating factor; MIC:
minimal inhibitory concentration; values in # represent
modulating factor [greater than or equal to] 2.

Table 4: Antibiotic resistance modulatory activity of
seeds extract of Dacryodes edulis.

                                  Bacteria MIC ([micro]g/mL) and
                                 modulating factors (in bracket)

                                       E. coli             E. aerogenes
                 Extract
Antibiotics    concentration       AG102       AG100Atet      EA27

CHL                  0              64             8           64
                   CMI/2       <2 ([greater      2 (4)#     32 (2)#
                              than or equal
                                 to] 32)#
                   CMI/4          8 (8)#         2 (4)#     32 (2)#
KAN                  0              32             4           16
                   CMI/2          8 (4)#         2 (2)#      8 (2)#
                   CMI/4          16 (2)#        2 (2)#     16 (0.5)
STP                  0              128           256         256
                   CMI/2          64 (2)#       128 (2)#    256 (1)
                   CMI/4          64 (2)#       256 (1)     256 (1)
CIP                  0               8             1           1
                   CMI/2           8 (1)        0.5 (2)#    2 (0.5)
                   CMI/4           8 (1)         2 (2)      2 (0.5)
TET                  0               8           < 0,5         64
                   CMI/2          2 (8)#       < 0,5 (na)    -(na)
                   CMI/4          2 (8)#       < 0,5 (na)    -(na)
ERY                  0              64             8           16
                   CMI/2          16 (4)#        2 (4)#      16 (1)
                   CMI/4          16 (4)#        2 (4)#      16 (1)

                                    Bacteria MIC ([micro]g/mL) and
                                    modulating factors (in bracket)

                                                                  P.
                              E. aerogenes   K. pneumoniae     stuartii
                 Extract
Antibiotics    concentration     EA289       KP55       KP 63    PS2636

CHL                  0             64         64         64        32
                   CMI/2         64 (1)     16 (4)#    16 (4)#   16 (2)#

                   CMI/4         64 (1)     32 (2)#    64 (1)    16 (2)#
KAN                  0             32         64         64        16
                   CMI/2         32 (1)     64 (1)     32 (2)#   2 (8)#
                   CMI/4         32 (1)     64 (1)     32 (2)#   2 (8)#
STP                  0             64         64         256       256
                   CMI/2         64 (1)    128 (0.5)   256 (1)   256 (1)
                   CMI/4         64 (1)    128 (0.5)   256 (1)   256 (1)
CIP                  0             1           8          4        16
                   CMI/2         1 (1)      2 (4)#     2 (2)#    4 (4)#
                   CMI/4         1 (1)      2 (4)#     2 (2)#    16 (1)
TET                  0             32         16         32         4
                   CMI/2         8 (4)#     1 (16)#    16 (2)#   1 (4)#
                   CMI/4         8 (4)#     2 (8)#     16 (2)#   1 (4)#
ERY                  0             64         64         32        16
                   CMI/2         64 (1)     16 (4)#    32 (1)     2 (8)
                   CMI/4         64 (1)     32 (2)#    32 (1)    16 (1)

                               Bacteria MIC ([micro]g/mL) and
                               modulating factors (in bracket)

                               P. stuartii    P. aeruginosa
                 Extract
Antibiotics    concentration      NEA16       PA01      PA124

CHL                  0             64          64        32
                   CMI/2         16 (4)#     32 (2)#   4 (8)#

                   CMI/4         32 (2)#     64 (1)    4 (8)#
KAN                  0             32          16        64
                   CMI/2         4 (8)#      8 (2)#    1 (64)#
                   CMI/4         8 (4)#      16 (1)    32 (2)
STP                  0             16          256       64
                   CMI/2         32 (2)#     256 (1)   1 (64)#
                   CMI/4         32 (2)#     256 (1)   32 (2)#
CIP                  0              2           2        16
                   CMI/2          2 (1)      1 (4)#    1 (16)#
                   CMI/4          2 (1)       2 (1)    4 (4)#
TET                  0             32          16        16
                   CMI/2         32 (1)      2 (8)#    1 (16)#
                   CMI/4         32 (1)      2 (8)#    4 (4)#
ERY                  0             32          16        32
                   CMI/2        64 (0.5)     8 (2)#    8 (4)#
                   CMI/4        64 (0.5)     8 (2)#    32 (1)

                               Bacteria MIC
                              ([micro]g/mL)
                              and modulating
                                 factors
                               (in bracket)

                 Extract        Modulating
Antibiotics    concentration    effect (%)

CHL                  0
                   CMI/2          90.00#

                   CMI/4          70.00#
KAN                  0
                   CMI/2          80.00#
                   CMI/4           60.00
STP                  0
                   CMI/2           40.00
                   CMI/4           20.00
CIP                  0
                   CMI/2           60.00
                   CMI/4           30.00
TET                  0
                   CMI/2          70.00#
                   CMI/4          70.00#
ERY                  0
                   CMI/2           60.00
                   CMI/4           40.00

CHL: chloramphenicol, KAN: kanamycin, STP: streptomycin, CIP:
ciprofloxacin, TET: tetracycline, ERY: erythromycin; -: MIC
not detected at up to 256 [micro]g/mL; ( ): modulating
factor; MIC: minimal inhibitory concentration; values in #
represent modulating factor [greater than or equal to] 2.

Table 5: Antibiotic resistance modulatory activity of
leaves extract of Ipomea batatas.

                               Bacteria MIC ([micro]g/mL) and
                               modulating factors (in bracket)

                              E. coli                E. aerogenes
Antibiotics      Extract
               concentration    AG102    AG100Atet      EA27

CHL                  0           64          8           64
                  CM 1/2       32 (2)#     8 (1)      16 (4)#
                   CMI/4       32 (2)#     8 (1)      32 (2)#
KAN                  0           32          4           16
                  CM 1/2       32 (1)      4 (1)       8 (2)#
                   CMI/4       32 (1)      4 (1)       8 (2)#
STP                  0           128        256         256
                  CM 1/2       64 (2)#    256 (1)     64 (4)#

                   CMI/4       64 (2)#    256 (1)     64 (4)#

CIP                  0            8          1           1
                   CMI/2       2 (4)#     0.5 (2)#     1 (1)

                   CMI/4       2 (4)#     0.5 (2)#     1 (1)

TET                  0            8        < 0.5         64
                   CMI/2        8 (1)    < 0.5 (na)    64 (1)
                   CMI/4        8 (1)    < 0.5 (na)    64 (1)
ERY                  0           64          8           16
                   CMI/2       16 (4)#     8 (1)       8 (2)#
                   CMI/4       16 (4)#     8 (1)       8 (2)#

                                   Bacteria MIC ([micro]g/mL) and
                                  modulating factors (in bracket)

                              E. aerogenes         K. pneumoniae
Antibiotics      Extract
               concentration      EA289        KP55          KP63

CHL                  0              64          64            64
                  CM 1/2          64 (1)      64 (1)        32 (2)#
                   CMI/4          64 (1)      64 (1)        16 (4)#
KAN                  0              32          64            64
                  CM 1/2          32 (1)      64 (1)        32 (2)#
                   CMI/4          32 (1)      64 (1)        32 (2)#
STP                  0              64          64            256
                  CM 1/2          64 (1)      32 (2)        64 (4)#

                   CMI/4         128 (1)      64 (1)        64 (4)#

CIP                  0              1            8             1
                   CMI/2          1 (1)        8 (1)    <0.5 ([greater
                                                        than or equal
                                                            to] 2)
                   CMI/4          1 (1)        8 (1)    <0.5 ([greater
                                                        than or equal
                                                            to] 4)
TET                  0              32          16            32
                   CMI/2          8 (4)#      16 (1)        32 (1)
                   CMI/4          8 (4)#      16 (1)        16 (2)#
ERY                  0              64          64            32
                   CMI/2          64 (1)      16 (4)#       16 (2)#
                   CMI/4          64 (1)      32 (2)        16 (2)#

                              Bacteria MIC ([micro]g/mL)
                               and modulating factors
                                    (in bracket)

                                    P. stuartii
Antibiotics      Extract
               concentration       PS2636        NEA16

CHL                  0               32           64
                  CM 1/2           32 (1)       32 (2)#
                   CMI/4           32 (1)       32 (2)#
KAN                  0               8            32
                  CM 1/2           4 (2)#       16 (2)#
                   CMI/4           4 (2)#       16 (2)#
STP                  0              >256          16
                  CM 1/2       128 ([greater    32 (2)#
                               than or equal
                                   to] 2)
                   CMI/4       256 ([greater    32 (2)#
                               than or equal
                                   to] 2)
CIP                  0               4             2
                   CMI/2           1 (4)#        2 (1)

                   CMI/4           2 (2)#        4 (1)

TET                  0               4            32
                   CMI/2           2 (2)#       4 (8)#
                   CMI/4           2 (2)#       16 (2)#
ERY                  0               16           32
                   CMI/2           2 (8)#       8 (4)#
                   CMI/4           4 (4)#       8 (4)#

                                  Bacteria MIC ([micro]g/mL) and
                                  modulating factors (in bracket)

                                   P. aeruginosa
Antibiotics      Extract                                  Modulating
               concentration        PA01          PA124    effect (%)

CHL                  0               64            32
                  CM 1/2           32 (2)#       16 (2)#     60.00
                   CMI/4           32 (2)#       16 (2)#     60.00
KAN                  0               16            64
                  CM 1/2           8 (2)#        16 (4)#     60.00
                   CMI/4           8 (2)#        32 (2)#     60.00
STP                  0               256           64
                  CM 1/2           64 (4)#       64 (1)      70.00#

                   CMI/4           64 (4)#       64 (1)      60.00

CIP                  0                2            16
                   CMI/2       <0.5 ([greater    16 (1)      40.00
                               than or equal
                                   to] 4)#
                   CMI/4       <0.5 ([greater    16 (1)      50.00
                               than or equal
                                   to] 4)#
TET                  0               16            16
                   CMI/2           4 (4)#        8 (2)#      50.00
                   CMI/4           4 (4)#        8 (2)#      60.00
ERY                  0               16            32
                   CMI/2           16 (1)        32 (1)      60.00
                   CMI/4           16 (1)        32 (1)      60.00

CHL: chloramphenicol, KAN: kanamycin, STP: streptomycin, CIP:
ciprofloxacin, TET: tetracycline, ERY: erythromycin; -: MIC
not detected at up to 256 [micro]g/mL; ( ): modulating factor; MIC:
minimal inhibitory concentration; values in # represent
modulating factor [greater than or equal to] 2.

Table 6: Antibiotic resistance modulatory activity of
leaves extract of Phaseolus vulgaris.

                                  Bacteria MIC ([micro]g/mL) and
                                  modulating factors (in bracket)

                                        E. coli             E. aerogenes
                 Extract
Antibiotics    concentration     AG102        AG100Atet        EA27

CHL                  0            64              8             64
                   CMI/2        32 (2)#        2 (4)#         64 (1)
                   CMI/4        32 (2)#        4 (2)#         64 (1)
KAN                  0            32              4             16
                   CMI/2        8 (4)#          4 (1)         8 (2)#
                   CMI/4        16 (2)#         4 (1)         8 (2)#
STP                  0            128            256           256
                   CMI/2        64 (2)#       128 (2)#       16 (16)#

                   CMI/4        64 (2)#        256 (1)       64 (4)#
CIP                  0             8              1             1
                   CMI/2         8 (1)     <0.5 ([greater     1 (1)
                                           than or equal
                                               to] 2)#
                   CMI/4         8 (1)       <0.5 (<0.5)      1 (1)
TET                  0             8            < 0.5           64
                   CMI/2       0.5 (16)#     < 0.5 (na)       64 (1)
                   CMI/4        4 (2)#       < 0.5 (na)       64 (1)
ERY                  0            64              8             16
                   CMI/2        16 (4)#        2 (4)#         16 (1)
                   CMI/4        16 (4)#        2 (4)#         16 (1)

                               Bacteria MIC ([micro]g/mL) and
                               modulating factors (in bracket)

                              E. aerogenes    K. pneumoniae
                 Extract
Antibiotics    concentration      EA289       KP55      KP 63

CHL                  0             64          64        64
                   CMI/2         32 (2)#     32 (2)#   32 (2)#
                   CMI/4         64 (1)      32 (2)#   32 (2)#
KAN                  0             32          64        64
                   CMI/2         32 (1)      64 (1)    16 (4)#
                   CMI/4         32 (1)      64 (1)    32 (2)#
STP                  0             64          64        256
                   CMI/2         32 (2)#     8 (8)#    4 (64)#

                   CMI/4         64 (1)      32 (2)#   8 (32)#
CIP                  0              1           8         1
                   CMI/2          1 (1)      4 (2)#     1 (1)

                   CMI/4          1 (1)      4 (2)#     1 (1)
TET                  0             32          16        32
                   CMI/2         16 (2)#     2 (8)#    8 (4)#
                   CMI/4         16 (2)#     8 (2)#    8 (4)#
ERY                  0             64          64        32
                   CMI/2         32 (2)#     32 (2)#   16 (2)#
                   CMI/4         32 (2)#     32 (2)#   16 (2)#

                                Bacteria MIC ([micro]g/mL) and
                               modulating factors (in bracket)

                                    P. stuartii         P. aeruginosa
                 Extract
Antibiotics    concentration      PS2636        NEA16     PA01

CHL                  0              32           64        64
                   CMI/2          8 (4)#       32 (2)#   64 (1)
                   CMI/4          8 (4)#       32 (2)#   64 (1)
KAN                  0               8           32        16
                   CMI/2          2 (4)#       16 (4)#   16 (1)
                   CMI/4          2 (4)#       16 (2)#   16 (1)
STP                  0             >256          16        256
                   CMI/2      256 ([greater    16 (1)    256 (1)
                              than or equal
                                  to] 2)#
                   CMI/4          256 (1)      16 (1)    256 (1)
CIP                  0               4            2         2
                   CMI/2           4 (1)        2 (1)     1 (2)

                   CMI/4           4 (1)        2 (1)     2 (1)
TET                  0               4           32        16
                   CMI/2          1 (4)#       32 (1)    2 (8)#
                   CMI/4          1 (4)#       32 (1)    2 (8)#
ERY                  0              16           32        16
                   CMI/2          4 (4)#       32 (1)    16 (1)
                   CMI/4          8 (2)#       32 (1)    16 (1)

                               Bacteria MIC ([micro]g/mL)
                                and modulating factors
                                    (in bracket)

                              P. aeruginosa
                 Extract                      Modulating
Antibiotics    concentration       PA124       effect (%)

CHL                  0              32
                   CMI/2          16 (2)#        80.00#
                   CMI/4          16 (2)#        70.00#
KAN                  0              64
                   CMI/2          16 (4)#        60.00
                   CMI/4          32 (2)#        60.00
STP                  0              64
                   CMI/2          64 (1)         70.00#

                   CMI/4          64 (1)         40.00
CIP                  0              16
                   CMI/2          16 (1)         30.00

                   CMI/4          16 (1)         10.00
TET                  0              16
                   CMI/2          8 (2)#         70.00#
                   CMI/4          8 (2)#         70.00#
ERY                  0              32
                   CMI/2          32 (1)         60.00
                   CMI/4          32 (1)         60.00

CHL: chloramphenicol, KAN: kanamycin, STP: streptomycin, CIP:
ciprofloxacin, TET: tetracycline, ERY: erythromycin; -: MIC
not detected at up to 256 [micro]g/mL; ( ): modulating factor; MIC:
minimal inhibitory concentration; values in # represent
modulating factor [greater than or equal to] 2.

Table 7: Antibiotic resistance modulatory activity of broad
bean extract of Theobroma cacao.

                               Bacteria MIC ([micro]g/mL) and
                               modulating factors (in bracket)

                                     E. coli         E. aerogenes
                 Extract
Antibiotics    concentration    AG102    AG100Atet     EA27

CHL                              64          8          64
                   CMI/2       32 (2)#     8 (1)      32 (2)#
                   CMI/4       32 (2)#     8 (1)      32 (2)#
KAN                  0           32          4          16
                   CMI/2       16 (2)#     4 (1)      8 (2)#
                   CMI/4       16 (2)#     4 (1)      8 (2)#
STP                  0           128        256         256
                   CMI/2       128 (1)     - (na)     256 (1)
                   CMI/4       128 (1)     - (na)     256 (1)
CIP                  0            8          1           1
                   CMI/2       4 (2)#      1 (1)       1 (1)
                   CMI/4       4 (2)#      1 (1)       2 (1)
TET                  0            8        < 0.5        64
                   CMI/2        8 (1)    < 0.5 (na)   64 (1)
                   CMI/4        8 (1)    < 0.5 (na)   64 (1)
ERY                  0           64          8          16
                   CMI/2       32 (2)#     8 (1)      8 (2)#
                   CMI/4       32 (2)#     8 (1)      16 (1)

                                Bacteria MIC ([micro]g/mL) and
                                modulating factors (in bracket)

                              E. aerogenes      K. pneumoniae
                 Extract
Antibiotics    concentration      EA289        KP55       KP 63

CHL                                64           64          64
                   CMI/2        128 (0.5)    128 (0.5)   16 (4)#
                   CMI/4        128 (0.5)    128 (0.5)    64 (1)
KAN                  0             32           64          64
                   CMI/2         64 (1)       64 (1)      64 (1)
                   CMI/4         64 (1)       64 (1)      64 (1)
STP                  0             64           64         256
                   CMI/2         64 (1)       32 (2)#    128 (2)
                   CMI/4        128 (2)#      32 (2)#    256 (1)
CIP                  0              1            8          1
                   CMI/2         0.5 (2)     16 (0.5)    0.5 (2)#
                   CMI/4          1 (1)      16 (0.5)    0.5 (2)#
TET                  0             32           16          32
                   CMI/2         16 (2)#      16 (2)#     8 (4)#
                   CMI/4         32 (1)       16 (1)     16 (2)#
ERY                  0             64           64          32
                   CMI/2        128 (0.5)     16 (4)#     8 (4)#
                   CMI/4        128 (0.5)     32 (2)#    16 (2)#

                               Bacteria MIC ([micro]g/mL) and
                               modulating factors (in bracket)

                                   P. stuartii       P. aeruginosa
                 Extract
Antibiotics    concentration     PS2636      NEA16      PA01

CHL                                32         64         64
                   CMI/2         8 (4)#     16 (4)#    64 (1)
                   CMI/4         8 (4)#     16 (4)#    64 (1)
KAN                  0             8          32         16
                   CMI/2         2 (4)#     8 (4)#     16 (1)
                   CMI/4         4 (2)#     16 (2)#    16 (1)
STP                  0            >256        16        256
                   CMI/2        32 (<8)#    16 (1)    256 (1)
                   CMI/4       16 (<16)#    16 (1)    256 (1)
CIP                  0             4           2         2
                   CMI/2       <0.5 (<8)#    2 (1)    0.5 (4)#
                   CMI/4       <0.5 (<8)#   4 (0.5)    1 (2)
TET                  0             4          32         16
                   CMI/2        0.5 (8)#    4 (8)#     8 (2)#
                   CMI/4        0.5 (8)#    4 (8)#     4 (4)#
ERY                  0             16         32         16
                   CMI/2         16 (1)     4 (8)#     16 (1)
                   CMI/4         16 (1)     16 (2)#    16 (1)

                              Bacteria MIC ([micro]g/mL)
                                and modulating factors
                                    (in bracket)

                              P. aeruginosa
                 Extract                     Modulating
Antibiotics    concentration      PA124       effect (%)

CHL                                 32
                   CMI/2          32 (1)        50.00
                   CMI/4          32 (1)        40.00
KAN                  0              64
                   CMI/2         32 (2)#        50.00
                   CMI/4         32 (2)#        50.00
STP                  0              64
                   CMI/2         32 (2)#        40.00
                   CMI/4         32 (2)#        40.00
CIP                  0              16
                   CMI/2          8 (2)         60.00
                   CMI/4          8 (2)         40.00
TET                  0              16
                   CMI/2          8 (2)#        70.00#
                   CMI/4          8 (2)#        50.00
ERY                  0              32
                   CMI/2         16 (2)#        60.00
                   CMI/4         16 (2)#        50.00

CHL: chloramphenicol, KAN: kanamycin, STP: streptomycin, CIP:
ciprofloxacin, TET: tetracycline, ERY: erythromycin; -: MIC
not detected at up to 256 [micro]g/mL; ( ): modulating factor; MIC:
minimal inhibitory concentration; values in # represent
modulating factor [greater than or equal to] 2.

Table 8: Antibiotic resistance modulatory activity of
leaves extract of Theobroma cacao.

                               Bacteria MIC ([micro]g/mL) and
                               modulating factors (in bracket)

                                     E. coli         E. aerogenes
                 Extract
Antibiotics    concentration    AG102    AG100Atet      EA27

CHL                  0           64          8           64
                   CMI/2       32 (2)#     2 (4)#     32 (2)#
                   CMI/4       32 (2)#     2 (4)#      64 (1)
KAN                  0           32          4           16
                   CMI/2       32 (1)      4 (1)       8 (2)#

                   CMI/4       32 (1)      4 (1)      32 (2)#
STP                  0           128        256         256
                   CMI/2       64 (2)#    128 (2)#    128 (2)#
                   CMI/4       128 (1)    256 (1)     128 (2)#
CIP                  0            8          1           1
                   CMI/2       4 (2)#      1 (1)       1 (1)

                   CMI/4        8 (1)      1 (1)      4 (0.25)

TET                  0            8        < 0.5         64
                   CMI/2        4 (2)    < 0.5 (na)   32 (2)#
                   CMI/4        8 (1)    < 0.5 (na)   32 (2)#
ERY                  0           64          8           16
                   CMI/2       32 (2)#     8 (1)       8 (2)#
                   CMI/4       32 (2)#     8 (1)       8 (2)#

                                  Bacteria MIC ([micro]g/mL) and
                                  modulating factors (in bracket)

                              E. aerogenes         K. pneumoniae
                 Extract
Antibiotics    concentration      EA289        KP55          KP 63

CHL                  0              64          64            64
                   CMI/2         16 (4)#      16 (4)#       32 (2)#
                   CMI/4          64 (1)      32 (2)        32 (2)#
KAN                  0              32          64            64
                   CMI/2         16 (2)#      32 (2)#       16 (4)#

                   CMI/4         16 (2)#      64 (1)        16 (4)#
STP                  0              64          64            256
                   CMI/2          64 (1)      32 (2)#       32 (4)#
                   CMI/4          64 (1)      64 (1)        32 (4)#
CIP                  0              1            8             1
                   CMI/2         0.5 (2)#      8 (1)    <0.5 ([greater
                                                        than or equal
                                                            to] 2)#
                   CMI/4          2 (2)       16 (2)    <0.5 ([greater
                                                        than or equal
                                                            to] 2)#
TET                  0              32          16            32
                   CMI/2         16 (2)#      16 (1)        16 (2)#
                   CMI/4         16 (2)#      16 (1)        16 (2)#
ERY                  0              64          64            32
                   CMI/2         128 (1)      32 (2)#       8 (2)#
                   CMI/4          64 (1)      32 (2)#       16 (4)#

                                 Bacteria MIC ([micro]g/mL) and
                                 modulating factors (in bracket)

                                     P. stuartii          P. aeruginosa
                 Extract
Antibiotics    concentration       PS2636        NEA16       PA01

CHL                  0               32            64         32
                   CMI/2           32 (1)       16 (4)#     32 (1)
                   CMI/4           8 (4)#       32 (2)#     32 (1)
KAN                  0               8             32         64
                   CMI/2       < 2 ([greater    16 (4)#     64 (1)
                               than or equal
                                  to] 4)#
                   CMI/4           2 (4)#       16 (2)#     64 (1)
STP                  0              256            16         32
                   CMI/2          8 (32)#        32 (1)     8 (4)#
                   CMI/4          128 (2)#       32 (1)    16 (2)#
CIP                  0               4             2          16
                   CMI/2          0.5 (8)#      0.5 (4)#    8 (2)#

                   CMI/4           4 (1)         2 (1)      8 (2)#

TET                  0               4             32         16
                   CMI/2           4 (1)         4 (8)#     8 (2)#
                   CMI/4           8 (2)#       16 (2)#     8 (2)#
ERY                  0               16            32         32
                   CMI/2           16 (1)        8 (4)#     8 (4)#
                   CMI/4           16 (1)        8 (4)#    16 (2)#

                              Bacteria MIC ([micro]g/mL)
                                and modulating factors
                                     (in bracket)

                              P. aeruginosa
                 Extract                      Modulating
Antibiotics    concentration       PA124       effect (%)

CHL                  0              64
                   CMI/2          64 (1)         70.00#
                   CMI/4          64 (1)         60.00
KAN                  0              16
                   CMI/2          16 (1)         60.00

                   CMI/4          16 (1)         50.00
STP                  0              256
                   CMI/2         128 (2)#        80.00#
                   CMI/4         128 (2)#        50.00
CIP                  0               2
                   CMI/2         0.5 (4)#        70.00#

                   CMI/4         0.5 (4)#        30.00

TET                  0              16
                   CMI/2          4 (4)#         70.00#
                   CMI/4          4 (4)#         70.00#
ERY                  0              16
                   CMI/2          8 (2)#         70.00#
                   CMI/4          16 (1)         60.00

CHL: chloramphenicol, KAN: kanamycin, STP: streptomycin, CIP:
ciprofloxacin, TET: tetracycline, ERY: erythromycin; -: MIC
not detected at up to 256 [micro]g/mL; ( ): modulating factor; MIC:
minimal inhibitory concentration; values in # represent
modulating factor [greater than or equal to] 2.

Table 9: Antibiotic resistance modulatory activity of barks
extract of Uapaca guineensis.

                              Bacteria MIC ([micro]g/mL) and
                              modulating factors (in bracket)

                                    E. coli         E. aerogenes
                 Extract
Antibiotics    concentration    AG102    AG100Atet    EA27

CHL                  0           64          8         64
                   CMI/2       32 (2)#     8 (1)     32 (2)#
                   CMI/4       32 (2)#     8 (1)     32 (2)#
KAN                  0           32          4         16
                   CMI/2       16 (2)#     4 (1)     8 (2)#
                   CMI/4       16 (2)#     4 (1)     8 (2)#
STP                  0           128        256        256
                   CMI/2       128 (1)    - (na)     256 (1)

                   CMI/4       128 (1)    - (na)     256 (1)

CIP                  0            8          1          1
                   CMI/2       4 (2)#      1 (1)      1 (1)

                   CMI/4       4 (2)#      1 (1)      1 (1)

TET                  0            8        < 0.5       64
                   CMI/2        8 (1)    <0.5 (na)   64 (1)
                   CMI/4        8 (1)    <0.5 (na)   64 (1)
ERY                  0           64          8         16
                   CMI/2       32 (2)#     8 (1)     8 (2)#
                   CMI/4       32 (2)#     8 (1)     16 (1)

                                Bacteria MIC ([micro]g/mL) and
                                modulating factors (in bracket)

                              E. aerogenes      K. pneumoniae
                 Extract
Antibiotics    concentration      EA289        KP55      KP 63

CHL                  0              64          64         64
                   CMI/2        128 (0.5)     64 (1)    16 (4)#
                   CMI/4        128 (0.5)     64 (1)     64 (1)
KAN                  0              32          64         64
                   CMI/2         64 (2)#      64 (1)    128 (1)
                   CMI/4         64 (2)#      64 (1)     64 (1)
STP                  0              64          64        256
                   CMI/2          64 (1)      32 (2)    128 (2)#

                   CMI/4         128 (2)#     32 (2)    256 (1)

CIP                  0              1            8         1
                   CMI/2         0.5 (2)#     16 (2)#   0.5 (2)

                   CMI/4          1 (1)       16 (2)#   0.5 (2)

TET                  0              32          16         32
                   CMI/2         16 (2)#      16 (2)#    8 (4)#
                   CMI/4          32 (1)      16 (1)    16 (2)#
ERY                  0              64          64         32
                   CMI/2          64 (1)      16 (4)#    8 (4)#
                   CMI/4          64 (1)      32 (2)#    16 (2)

                                 Bacteria MIC ([micro]g/mL) and
                                 modulating factors (in bracket)

                                       P. stuartii        P. aeruginosa
                 Extract
Antibiotics    concentration       PS2636         NEA16      PA01

CHL                  0               32            64         64
                   CMI/2           8 (4)#        16 (4)#    64 (1)
                   CMI/4           8 (4)#        16 (4)#    64 (1)
KAN                  0                8            32         16
                   CMI/2           2 (4)#        8 (4)#     16 (1)
                   CMI/4           4 (2)#        16 (2)#    16 (1)
STP                  0              >256           16        256
                   CMI/2        32 ([greater     16 (1)    256 (1)
                               than or equal
                                   to] 8)#
                   CMI/4        16 ([greater     16 (1)    256 (1)
                               than or equal
                                   to] 8)#
CIP                  0                4             2         2
                   CMI/2       <0.5 ([greater     2 (1)    0.5 (4)#
                               than or equal
                                   to] 8)#
                   CMI/4       <0.5 ([greater     2 (1)     1 (2)#
                               than or equal
                                   to] 8)#
TET                  0                4            32         16
                   CMI/2          0.5 (8)#       4 (8)#     8 (2)#
                   CMI/4          0.5 (8)#       4 (8)#     4 (4)#
ERY                  0               16            32         16
                   CMI/2           16 (1)        4 (8)#     16 (1)
                   CMI/4           16 (1)        16 (2)#    16 (1)

                               Bacteria MIC ([micro]g/mL)
                                and modulating factors
                                      (in bracket)

                              P. aeruginosa
                 Extract                      Modulating
Antibiotics    concentration       PA124       effect (%)

CHL                  0              32
                   CMI/2          32 (1)         50.00
                   CMI/4          32 (1)         40.00
KAN                  0              64
                   CMI/2          32 (2)#        60.00
                   CMI/4          32 (2)#        60.00
STP                  0              64
                   CMI/2          32 (2)#        40.00

                   CMI/4          32 (2)#        40.00

CIP                  0              16
                   CMI/2          8 (2)#         70.00#

                   CMI/4          8 (2)#         60.00

TET                  0              16
                   CMI/2          8 (2)#         70.00#
                   CMI/4          8 (2)#         50.00
ERY                  0              32
                   CMI/2          16 (2)#        60.00
                   CMI/4          16 (2)#        50.00

CHL: chloramphenicol, KAN: kanamycin, STP: streptomycin, CIP:
ciprofloxacin, TET: tetracycline, ERY: erythromycin; -: MIC
not detected at up to 256 [micro]g/mL; ( ): modulating factor; MIC:
minimal inhibitory concentration; values in # represent
modulating factor [greater than or equal to] 2.
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Title Annotation:Research Article
Author:Nayim, Paul; Mbaveng, Armelle T.; Wamba, Brice E.N.; Fankam, Aime G.; Dzotam, Joachim K.; Kuete, Vic
Publication:The Scientific World Journal
Date:Jan 1, 2018
Words:9063
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