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Antistaphylococcal and Antibiotic Resistance Modulatory Activities of Thirteen Cameroonian Edible Plants against Resistant Phenotypes.

1. Background

Bacterial infections caused by Staphylococcus aureus are globally responsible for 7-10% of deaths annually [1]. It is the most virulent species of the genus Staphylococcus and has emerged as one of the most important human pathogens in the last decades, being one of the main causes of hospital and community infections [2]. This bacterium causes a wide range of clinical infections, ranging from common infections such as skin and soft tissue infections to septicemia, pneumonia, and toxinosis [3,4]. The fight against S. aureus is hindered by the development of resistance of various strains to antibiotics [5-9]. The multidrug resistance (MDR) observed in Gram-positive bacteria is mostly attributed to overexpression of efflux pumps and antibiotics-degrading enzymes. This MDR of S. aureus propels the search of new antibacterials with more efficiency and low toxicity. Plant kingdom contains a variety of pharmacologically active secondary metabolites, and some of them have been reported for their antibacterial activities [10, 11]. Their use to combat S. aureus antibiotic resistance is an attractive strategy. In regard to the loss of efficacy of several antibiotics and the scarcity of new antibacterial agents, it is also important to search for substances capable of restoring the activity of antibiotics. Antibacterial screenings of African plants have yielded promising results in the past [12-15]. The present study was set up to evaluate the antistaphylococcal potential of 13 Cameroonian food plants: Azadirachta indica A. Juss (Meliaceae), Citrus grandis (L.) Osbeck (Rutaceae), Cucurbita maxima Duch. (Cucurbitaceae), Dacryodes edulis (G. Don) H. J. Lam (Burseraceae), Hibiscus esculentus L. (Malvaceae), Ipomoea batatas (L.) Lam (Convolvulaceae), Irvingia gabonensis (Aubry. Lec. ex O. Rorke) Baill. (Irvingiaceae), Phaseolus vulgaris L. (Fabaceae), Ricinodendron heudelotii (Baill.) Pierre ex Heckel (Euphorbiaceae), Saccharum officinarum L. (Poaceae), Spondias mombin L. (Anacardiaceae), Theobroma cacao L. (Sterculiaceae), and Uapaca guineensis Muell. Arg. (Euphorbiaceae). The study was extended on the role of efflux pumps in resistance to some plant extracts as well as the ability of extracts to potentiate the activity of selected antibiotics.

2. Materials and Methods

2.1. Plant Materials and Extraction. The thirteen edible plants were collected from different localities of Cameroon, namely, Obala (Centre Region), Muyuka (South-West Region), and Dschang (West Region) from March to April 2016. The collected plant samples included the bark of Azadirachta indica A. Juss (Meliaceae), leaves of Citrus grandis (L.) Osbeck (Rutaceae), beans of Cucurbita maxima Duch. (Cucurbitaceae), leaves, bark, and seeds of Dacryodes edulis (G. Don) H. J. Lam (Burseraceae), leaves of Hibiscus esculentus L. (Malvaceae), beans of Ipomoea batatas (L.) Lam (Convolvulaceae), leaves of Irvingia gabonensis (Aubry. Lec. ex O. Rorke) Baill. (Irvingiaceae), leaves of Phaseolus vulgaris L. (Fabaceae), bark and leaves of Ricinodendron heudelotii (Baill.) Pierre ex Heckel (Euphorbiaceae), leaves of Saccharum officinarum L. (Poaceae), leaves of Spondias mombin L. (Anacardiaceae), leaves and beans of Theobroma cacao L. (Sterculiaceae), and leaves and bark of Uapaca guineensis Muell. Arg. (Euphorbiaceae). Plants were identified at the National Herbarium in Yaounde (Cameroon) where the voucher specimens were conserved under the registration numbers (Table 1). The dried and powdered material (100 g) of each plant was macerated in 300 mL of methanol at room temperature for 48 h and then filtered using Whatman filter paper No. 1. The filtrate obtained was concentrated using a rotary evaporator under reduced pressure to obtain the crude methanol extract, which was kept at 4[degrees]C until further use.

2.2. Chemicals. Eight reference antibiotics (RA) purchased from Sigma-Aldrich (St Quentin Fallavier, France) were tested: ampicillin (AMP), cefepime (CEF), chloramphenicol (CHL), ciprofloxacin (CIP), erythromycin (ERY), kanamycin (KAN), streptomycin (STR), and tetracycline (TET); p-iodonitrotetrazolium chloride (INT) (Sigma-Aldrich) was used as bacterial growth revelator; carbonyl cyanide m-chlorophenyl hydrazone (CCCP) and chlorpromazine (CPZ) (Sigma-Aldrich) were used as efflux pump inhibitors (EPIs); and dimethylsulfoxide (DMSO) was used to dissolve the plant extracts.

2.3. Bacteria, Culture Media, and Growth Conditions. The strains of Staphylococcus aureus used included a reference strain obtained from American Type Culture Collection (ATCC; ATCC 25923), 8 methicillin-resistant S. aureus (MRSA) strains (MSSA1, MRSA3, MRSA4, MRSA6, MRSA8, MRSA9, MRSA11, and MRSA12) (obtained from the culture collection of the Laboratory of Microbiology, Graduate School of Pharmaceutical Sciences, The University of Tokyo, Japan, and provided by Dr Jean P. Dzoyem, University of Dschang) [8, 9], and 17 resistant clinical laboratory strains of S. aureus (SA01, SA07, SA18, SA23, SA36, SA39, SA56, SA64, SA68, SA88, SA114, SA116, SA124, SA126, SA127, SA135, and SA139) available in our laboratory collection and previously isolated from patients in Ad-Lucem Hospital in Banka-Bafang (West Region of Cameroon) [54]. Their bacterial features are summarized in Table 2. They were cultured at 37[degrees]C overnight on Mueller Hinton agar 24 h prior to any assay. The Mueller Hinton broth (MHB) was used as liquid culture medium for susceptibility tests.

2.4. Preliminary Phytochemical Screenings. Potential classes of potential antibacterial phytochemicals such as alkaloids (Dragendorffs and Mayer's tests: 5 mg plant extract in 10 mL methanol; a portion of 2 mL extract +1% HCl + steam, 1 mL filtrate+ 6 drops of Mayor's reagents/Wagner's reagent/-Dragendorff's reagent; cream precipitate/brownish-red precipitate/orange precipitate indicated the presence of respective alkaloids), saponins (frothing test: 0.5 mL filtrate + 5 mL distilled water; frothing persistence indicated the presence of saponins), steroids and triterpenoids (Liebermann-Burchard test: 5 mg plant extract in 10 mL chloroform, filtered; a 2 mL filtrate + 2 mL acetic anhydride + conc. [H.sub.2]S[O.sub.4]; blue-green ring or pink-purple indicated the presence of steroids or triterpenoids), phenolics: anthraquinones (5 mg plant extract in 10 mL methanol; a portion of 2mL + 2mL ether-chloroform 1:1 v/v+4mL NaOH 10% (w/v); red color indicated the presence of anthraquinones), flavonoids (5 mg plant extract in 10 mL methanol; a portion of 2 mL + conc. HCl + magnesium; ribbon pink-tomato red color indicated the presence of flavonoids), polyphenols (ferric chloride test: 5 mg plant material in 10 mL methanol; a portion of 2 mL + 2 mL Fe[Cl.sub.3]; violet-blue or greenish color indicated the presence of phenols), and tannins (5 mg plant extract in 10 mL distilled water; a portion of 2 mL + 2 mL Fe[Cl.sub.3]; blue-black precipitate indicated the presence of tannins) (Table 3) were investigated according to the described phytochemical methods [11, 55].

2.5. INT Colorimetric Assay for MIC and Minimal Bactericidal Concentration (MBC) Determinations. The MIC and minimal bactericidal concentration (MBC) determinations on various strains of S. aureus were performed using the rapid INT colorimetric assay [56] with some modifications as previously described [14, 38]. The samples were dissolved in DMSO/MHB. The final concentration of DMSO was lower than 2.5%. The twofold dilutions of the samples were made in a 96-well microplate, and the tested bacterial concentration was 1.5 x [10.sup.6] colony-forming unit (CFU)/mL. The microplates were incubated at 37[degrees]C for 18 h. All assays were performed in triplicate and repeated thrice. Wells containing MHB, 100 [micro]L of inoculum, and DMSO to a final concentration of 2.5% served as negative control. The MIC of each sample was detected after 18 h incubation at 37[degrees]C, following addition (40 [micro]L) of 0.2 mg/mL of INT and incubation at 37[degrees]C for 30 minutes as the lowest sample concentration that prevented the color change of the medium and exhibited complete inhibition of microbial growth [56]. The MBC 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. These preparations were further 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 [57, 58].

2.6. Evaluation of the Role of Efflux Pumps in the Resistance of Selected Bacteria. To evaluate the involvement of efflux pumps in the resistance of selected bacterial strains to some of the active plant extracts, Dacryodes edulis seeds (DES), Hibiscus esculentus leaves (HEL), Uapaca guineensis leaves (UGL), Uapaca guineensis bark (UGB), and CIP (reference drug) were tested in the absence or presence of EPI (CCCP (0.5 [micro]g/mL) or CPZ (25 [micro]g/mL)). MICs of samples alone or in combination with EPI were determined as above, and the increase in activity was determined as the ratio of MIC of sample alone versus sample in combination with EPI. All assays were performed in triplicate and repeated thrice.

2.7. Antibiotic Activity Modulation Assays. To evaluate the antibiotic resistance modulation activity of the most active extracts: Azadirachta indica bark (AIB), Dacryodes edulis seeds (DES), Dacryodes edulis bark (DEB), Dacryodes edulis leaves (DEL), Phaseolus vulgaris leaves (PVL), Ricinodendron heudelotii leaves (RHL), and Uapaca guineensis bark (UGB), a preliminary assay was performed in order to assess the MICs of antibiotics in the absence and presence of these extracts using the broth microdilution method as previously described [14,38, 56]. S. aureus SA88 was used for the preliminary assay, and the samples were tested at various subinhibitory concentrations (MIC/2, MIC/4, MIC/8, and MIC/16). Results allowed to select DEB, DEL, DES, RHL, and UGB to be tested further against S. aureus ATCC 25923, and 8 resistant strains of S. aureus (MRSA3, MRSA4, MRSA9, MRSA11, MRSA12, SA18, SA36, and SA64) at MIC/2 and MIC/4. Briefly, after serial dilutions of antibiotics, extract was added to each well at its subinhibitory concentrations, the bacterial inoculation was done, and the MIC was determined. Rows receiving antibiotic dilutions without extracts were used for the determination of the MICs of the antibiotics. The modulation factor was defined as the ratio of the MIC of antibiotic alone versus that of antibiotic in the presence of extract. Modulation factor [greater than or equal to] 2 was set as the cutoff for biologically significance of antibiotic resistance-modulating effects [59].

3. Results

3.1. Phytochemical Composition of Plant Extracts. The major classes of phytochemicals were screened in the 18 studied plant extracts (Table 3). It appears that all extracts contained polyphenols and tannins. Other classes of phytochemicals were selectively present. Only the extract of the beans of Theobroma cacao contained all the investigated classes of secondary metabolites.

3.2. Antibacterial Activity. The antibacterial activities of the 18 tested extracts and ciprofloxacin against 26 strains of S. aureus are summarized in Table 4. It appears that extracts from Dacryodes edulis seeds (DES) and Dacryodes edulis bark (DEB), within a MIC range of 256-1024 [micro]g/mL, and ciprofloxacin (MIC below 4 [micro]g/mL), were active against all 26 tested bacterial strains. Other extracts were selectively active, and MIC values varied from 64 to 1024 [micro]g/mL against 25/26 (96.2%) tested bacteria for Phaseolus vulgaris leaves (PVL), 24/26 (92.3%) for Azadirachta indica bark (AIB), Dacryodes edulis leaves (DEL), and Ricinodendron heudelotii leaves (RHL), 23/26 (88.5%) for Hibiscus esculentus leaves (HEL), 19/26 (73.1%) for Uapaca guineensis leaves (UGL), 18/26 (69.2%) for Ricinodendron heudelotii bark (RHB) and Uapaca guineensis bark (UGB), 17/26 (61.5%) for Saccharum officinarum leaves (SOL), 16/26 (61.5%) for Ipomoea batatas leaves (IBL) and Theobroma cacao leaves (TCL), 15/26 (57.7%) for Citrus grandis leaves (CGL), 14/26 (53.8%) for Theobroma cacao beans (TCB), 12/26 (46.2%) for Cucurbita maxima beans (CMB), 10/26 (38.5%) for Spondias mombin leaves (SML), and 7/26 (26.9%) for Irvingia gabonensis beans (IGB). The lowest MIC value of 64 [micro]g/mL was obtained with CMB against MRSA4 strain and UGB against MRSA9 strain.

3.3. Role of Efflux Pumps in the Resistance of Strains of S. aureus. Four extracts (DES, HEL, UGL, and UGB) and CIP (reference drug) were tested in the absence or presence of CCCP (0.5 [micro]g/mL) and CPZ (25 [micro]g/mL) to evaluate the role of efflux pumps in the resistance of 14 tested S. aureus strains. The results are summarized in Tables 5 and 6. It appears that CCCP significantly improved the activity of the 4 tested extracts against the majority of S. aureus strains (Table 5). The increase of activity in the presence of CCCP ranged from 2-fold to > 128-fold. The highest increase of activity (> 128-fold) was obtained when DES, UGB, and UGL were tested in the presence of CCCP on at least one S. aureus strain. In contrast, in the presence of CPZ, no improvement in the activity of the four extracts was observed (Table 6). This is clear indication that CCCP was the appropriate EPI of the studied S. aureus strains.

3.4. Antibiotic Resistance Modulation Activity of Extracts. Seven plant extracts, AIB, DES, DEB, DEL, PVL, RHL, and UGB, at their various subinhibitory concentrations (MIC/2, MIC/4, MIC/8, and MIC/16) were first tested in combination with 8 antibiotics: CHL, TET, CIP, AMP, CEF, ERY, STR, and KAN against S. aureus SA88 strain. The results summarized in Table S1 (Supplementary Materials) show that better modulation of the activity of antibiotics was obtained with all extracts at MIC/2 and MIC/4. At their MIC/2, 2-fold or more increase of antibiotic activities was obtained with PVL, AIB, DEB, DES, DEL, UGB, and RHL and 2, 4, 4, 6, 6, 7, and 8 of the 8 tested antibiotics, respectively (Table S1; Supplementary Materials). Consequently, the most active extracts, DEB, DEL, DES, RHL, and UGB, were further tested in combination with the above 8 antibiotics against the reference strains (ATCC 25923) and 8 resistant strains of S. aureus at MIC/2 and MIC/4 (Tables S2-S6; Supplementary Materials). Results showed that 2-fold or more antibiotic-modulating effects against more than 70% of the S. aureus strains tested were obtained when DEB was combined with CHL at MIC/2 (77.78%; Table S2; Supplementary Materials), when DEL was combined with CHL and STR at MIC/2 (77.78%; Table S3; Supplementary Materials), when DES was combined with CIP (77.78% at MIC/2), CHL (100% and 88.89 at MIC/2 and MIC/4 resp.), TET (77.78% at MIC/2 and MIC/4), and STR (88.89% and 77.78% at MIC/2 and MIC/4 resp.) (Table S4; Supplementary Materials), when RHL was combined with CIP, ERY, and KAN (88.89% and 77.78% at MIC/2 and MIC/4 resp.), CHL (88.89% at MIC/2 and MIC/4), TET (77.78% at MIC/2 and MIC/4), and STR (88.89% at MIC/2) (Table S5; Supplementary Materials), and when UGB was combined with CHL, KAN, and STR (77.78% at MIC/2 and MIC/4) (Table S6; Supplementary Materials).

4. Discussion

4.1. Phytochemical Composition of Extracts. Polyphenols and tannins were detected in all extracts. The role of several molecules belonging to polyphenols as antibacterials has been demonstrated [10, 11, 38, 61]. Tannins also belong to a class of polyphenols, and its presence in all extracts could in part explain the fact that all the tested extracts were active in at least one strain of the tested bacteria [10]. However, it should be made clear that the presence of a class of secondary metabolite with reported antibacterial effect is not a guarantee of the good activity of a plant. The antibacterial effect depends on the structure and the amount of a particular phytochemical in the plant or possible interactions with other compounds. This could explain why the extract from the beans of Theobroma cacao that contained all the investigated classes of secondary metabolites (Table 3) was not the most active sample (Table 4).

4.2. Antibacterial Potential of Extracts. Resistance of bacteria to antibiotics propels the search of new agents to fight against MDR phenotypes. In the present study, clinical strains of S. aureus used were previously reported as resistant to at least one commonly used antibiotic [8, 9] (Table 2). Several locally isolated strains of S. aureus [54] were used herein, to better adapt the study to our environment. According to established criteria, MIC values in the range of 100-1000 [micro]g/mL are indication that plant extracts bear antimicrobial activities [62]. Also, the antibacterial activity of botanicals is considered significant if MIC values are below 100 [micro]g/mL, moderate if 100 [less than or equal to] MICs [less than or equal to] 625 [micro]g/mL, and weak if MICs > 625 [micro]g/mL [37, 60]. On these bases, it can be deduced that all the tested plant extracts had antistaphylococcal activities, except Irvingia gabonensis beans (IGB), with MICs above 1000 [micro]g/mL against all tested strains of S. aureus (Table 4). This activity was significant for CMB against MRSA4 strain and UGB against MRSA9 strain (MIC: 64 [micro]g/mL). Most of the recorded MIC values ranged from 512 to 1024 [micro]g/mL, indicating that extracts rather exhibited moderate to low antistaphylococcal effects. However, this activity could be considered important because the clinical strains of S. aureus used were resistant phenotypes while extracts were from edible plants. In effect, it was suggested that if botanicals are food plants, as they are allegedly nontoxic or less toxic than other medicinal plants, their antibacterial activity is significant in a range of 100 [less than or equal to] MIC [less than or equal to] 512 [micro]g/mL and moderately active in a range of 512 < MIC [less than or equal to] 2048[micro]g/mL [63].

4.3. Role of Efflux Pumps in Susceptibility of S. aureus Strains to the Extracts. Bacterial efflux systems are associated with major human health concerns as they are involved in the resistance of pathogenic bacteria such as S. aureus [64-66]. Previously, inhibition of efflux pumps by natural products has been found to improve the activity of antibiotics against S. aureus. For example, inhibition of the TetK efflux pump was reported with the essential oil of Chenopodium ambrosioides and its constituent [alpha]-terpinene against S. aureus IS-58 strain [66]. In the present study, two well-known EPIs (CCCP and CPZ) were used to assess the implication of efflux pumps in the resistance of the studied S. aureus strains to plant extracts. CCCP is an inhibitor of the proton-motive force of ATP-binding cassette (ABC) transporters of several Gram-negative and Gram-positive bacteria, including S. aureus [5-7]. CPZ is capable of reversing or reducing the antibiotic resistance of bacteria including S. aureus [67], due to its indirect effects on ATPase activity that is dependent upon [Ca.sup.2+] [68]. In the present study, it was found that CCCP contrary to CPZ improved the activity of the four extracts (DES, HEL, UGL, and UGB) (Tables 5 and 6). This indicates that ABC transporters are involved in the resistance of the studied strains of S. aureus and that combination of extracts such as HEL, UGL, and UGB with an inhibitor of ABC transporters could improve the antistaphylococcal fight.

4.4. Antibiotic Modulation Effects of Extracts. The antibiotic resistance-modulating effects of several botanicals and phytochemicals against resistant bacteria have been documented [12-15, 59, 69]. It has been suggested that extracts capable of potentiating the activity of antibiotics on more than 70% of bacteria could be potential efflux pump inhibitors [70]. In this study, antibiotic modulation activity of extracts at their MIC/2 on more than 70% tested strains of S. aureus was obtained with the association of DEB and DEL and with 1/8 (12.5%) tested antibiotics (Tables S2 and S3; Supplementary Materials), UGB with 2/8 (25%) antibiotics (Table S6; Supplementary Materials), DES with 4/8 (50%) antibiotics (Table S4; Supplementary Materials), and RHL with 6/8 (75%) antibiotics (Table S5; Supplementary Materials). Hence, the tested extracts and mostly RHL may act as efflux pump inhibitors [70]. The use of CCCP indicated that ABC transporters were the efflux pumps involved in the resistance of the tested bacteria, suggesting that the above extract could be the inhibitors of such pumps. The potential of the R. heudelotii leaf extract (RHL) to reverse antibiotic resistance in Gram-negative MDR bacteria was previously reported [18]. The present study therefore provides more information about the ability of this plant to modulate the activity of antibiotics against resistant strains of S. aureus.

5. Conclusion

In conclusion, the present work provides informative data about the antistaphylococcal potential of 13 Cameroonian food plants. It also indicates that some extracts such as DES, HEL, UGL, and UGB could be used in combination with EPI to combat resistance of Staphylococcus aureus to antibiotics. Finally, this study also demonstrates that some studied extracts and mostly RHL could be used as antibiotic resistance modulators, providing a new weapon against the resistance of S. aureus to antibiotics.

https://doi.org/10.1155/2018/1920198

Abbreviations

AIB: Azadirachta indica bark

AMP: Ampicillin

ATCC: American Type Culture Collection

CCCP: Carbonyl cyanide m-chlorophenyl hydrazone

CEF: Cefepime

CFU: Colony-forming unit

CGL: Citrus grandis

CHL: Chloramphenicol

CIP: Ciprofloxacin

CMB: Cucurbita maxima beans

CPZ: Chlorpromazine

DEB: Dacryodes edulis bark

DEL: Dacryodes edulis leaves

DES: Dacryodes edulis seeds

DMSO: Dimethylsulfoxide

EPI: Efflux pump inhibitors

ERY: Erythromycin

HEL: Hibiscus esculentus leaves

IBL: Ipomoea batatas leaves

IGB: Irvingia gabonensis beans

INT: p-Iodonitrotetrazolium chloride

KAN: Kanamycin

MBC: Minimal bactericidal concentration

MDR: Multidrug-resistant

MHB: Mueller Hinton broth

MIC: Minimal inhibitory concentration

MRSA: Methicillin-resistant Staphylococcus aureus

PVL: Phaseolus vulgaris leaves

RA: Reference antibiotics

RHB: Ricinodendron heudelotii bark

RHL: Ricinodendron heudelotii leaves

SA: Staphylococcus aureus

SML: Spondias mombin leaves

SOL: Saccharum officinarum leaves

STR: Streptomycin

TCB: Theobroma cacao beans

TCL: Theobroma cacao leaves

TET: Tetracycline

UGB: Uapaca guineensis bark

UGL: Uapaca guineensis leaves.

Data Availability

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

Conflicts of Interest

The authors declare that they have no conflicts of interest.

Authors' Contributions

Brice E. N. Wamba, Paul Nayim, Joachim K. Dzotam, and Ornella J. T. Ngalani carried out the study. Armelle T. Mbaveng and Victor Kuete designed the experiments. Armelle T. Mbaveng and Victor Kuete wrote the manuscript. Armelle T. Mbaveng and Victor Kuete supervised the work and provided the bacterial strains. All authors read and approved the final manuscript.

Acknowledgments

The authors are thankful to the Cameroon National Herbarium for identification of plants and also thank Dr. Jean P. Dzoyem (University of Dschang, Cameroon) for providing the MRSA strains of S. aureus.

Supplementary Materials

Preliminary evaluation of antibiotic resistance modulatory activity of extracts against S. aureus SA88 (Table S1); antibiotic resistance modulatory activity of the bark methanol extract from Dacryodes edulis bark (DEB) (Table S2); the leaf methanol extract from Dacryodes edulis leaves (DEL) (Table S3); the seed methanol extract from Dacryodes edulis seeds (DES) (Table S4); the leaf methanol extract from Ricinodendron heudelotii leaves (RHL) (Table S5); and the bark methanol extract from Uapaca guineensis bark (UGB) (Table S6) at their MIC/2 and MIC/4 on selected strains of Staphylococcus aureus. (Supplementary Materials)

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Brice E. N. Wamba, Armelle T. Mbaveng, Paul Nayim, Joachim K. Dzotam, Ornella J. T. Ngalani, and Victor Kuete

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

Correspondence should be addressed to Victor Kuete; kuetevictor@yahoo.fr

Received 24 March 2018; Accepted 6 June 2018; Published 3 July 2018

Academic Editor: Clemencia Chaves-Lopez
Table 1: Information on the studied plants.

Species (family);
voucher
number                    Traditional uses

Azadirachta                Antimalarial,
indica A. Juss              anticancer,
(Meliaceae);             antiinflammatory,
4447/SRFK                   antidiabetic,
                        antihyperglycaemic,
                          antiulcerous [16]

Citrus grandis             Cancer [19, 20]
(L.) Osbeck
(Rutaceae);
25,860/SRFC

Cucurbita                 Diabetes, cancer,
maxima Duch.             antihypertensive,
(Cucurbitaceae);          antiinflammatory,
42,449/HNC               immunomodulating,
                           and bacterial
                         infections [22, 23]

Dacryodes edulis          Gastrointestinal
(G. Don) H. J.               disorders,
Lam (Burseraceae);       toothache, earache
1874/SRFK                 [27], dysentery,
                          anemia, leprosy,
                        [28], skin diseases,
                           and sickle cell
                            disease [29]

Hibiscus                   Inflammation,
esculentus L.            pain [30], cancer,
(Malvaceae);              hypoglycemic [31]
42,823/HNC

Ipomoea                    Antidiabetic,
batatas (L.) Lam         anti-inflammatory,
(Convolvulaceae);         reducing risk of
55,594/HNC                 cardiovascular
                        disease, anticancer,
                          reducing stomach
                          stress, nausea,
                            diarrhea [32]

Irvingia gabonensis      Diarrhea, hernia,
(Aubry. Lec. ex O.          yellow fever,
Rorke) Baill.                dysentery,
(Irvingiaceae);         antipoison [35, 36],
52,936/HNC                   gonorrhea,
                        gastrointestinal and
                         hepatic disorders,
                         wound infections,
                             diabetes,
                           analgesic [37]

Phaseolus                Antioxidant [39],
vulgaris                cancer, estrogenic,
L. (Fabaceae);          antidepressant [40],
42,587/HNC             bacterial infections,
                          tuberculosis [41]

Ricinodendron             Cough, antidote,
heudelotii (Baill.)     intestinal diseases
Pierre ex Heckel         [43], yellow fever,
(Euphorbiaceae);          malaria, stomach
50,852/HNC                pain, headache,
                           dysentery [44]

Saccharum                   Jaundice and
officinarum L.             liver problems,
(Poaceae);                  hemorrhoids,
42,958/HNC                   dysentery,
                          menorrhagia [45]

Spondias                     Diuretic,
mombin L.                    febrifuge,
(Anacardiaceae);              diarrheal
21,249/SRFK             diseases, dysentery,
                            hemorrhoids,
                             gonorrhea,
                           leucorrhea [47]

)eobroma cacao L.         Cardiovascular,
(Sterculiaceae);          gastrointestinal,
60,111/HNC                  and nervous
                            diseases [49]

Uapaca guineensis        Leprosy, epilepsy,
Muell. Arg.              edema, rheumatism,
(Euphorbiaceae);         aphrodisiac, fever,
53,136/HNC                 inflammation,
                           absorption [52]

                            Bioactive or
Species (family);            potentially
voucher                       bioactive
number                        components

Azadirachta                  Alkaloids,
indica A. Juss               glycosides,
(Meliaceae);                 flavonoids,
4447/SRFK                 and saponins [17]

Citrus grandis               Alkaloids,
(L.) Osbeck               cardioglycosides,
(Rutaceae);              saponins, tannins,
25,860/SRFC                  terpenoids,
                           flavonoids, and
                            steroids [21]

Cucurbita                Tannins, saponins,
maxima Duch.               alkaloids [24],
(Cucurbitaceae);          cucurbitaxanthin,
42,449/HNC                gibberellin, and
                               [alpha]-
                           tocopherol [25]

Dacryodes edulis            Ethyl gallate
(G. Don) H. J.           and quercitrin [27]
Lam (Burseraceae);
1874/SRFK

Hibiscus                     Not reported
esculentus L.
(Malvaceae);
42,823/HNC

Ipomoea                    Caffeoylquinic
batatas (L.) Lam          acid [33], vitamin
(Convolvulaceae);         E, beta-carotene,
55,594/HNC                 lutein, saponins
                          [32], flavonoids,
                         and chitinases [34]

Irvingia gabonensis      Saponins, tannins,
(Aubry. Lec. ex O.           phenols, and
Rorke) Baill.            phlobatannins [35],
(Irvingiaceae);               alkaloids,
52,936/HNC               cardiac glycosides,
                           anthraquinones,
                              tannins,
                          flavonoids [36],
                           3-friedelanone;
                           betulinic acid;
                           oleanolic acid;
                             3,3,4-tri-O-
                         methylellagic acid;
                       3,4-di-O-methylellagic
                          acid; hardwickiic
                              acid [38]

Phaseolus                    Alkaloids,
vulgaris                    steroids, and
L. (Fabaceae);             flavonoids [42]
42,587/HNC

Ricinodendron           Tannins, polyphenols,
heudelotii (Baill.)    alkaloids, glycosides,
Pierre ex Heckel        flavonoids, steroids,
(Euphorbiaceae);         and saponins [43],
50,852/HNC                aleuritolic acid,
                        labda-8(17), 13-diem-
                          3[beta], 15-diol,
                            E-ferulic acid
                          octacosylate [44]

Saccharum                    Flavonoids,
officinarum L.            saponins, tannins,
(Poaceae);                and alkaloids [46]
42,958/HNC

Spondias                 Saponins, tannins,
mombin L.                    flavonoids,
(Anacardiaceae);           alkaloids, and
21,249/SRFK                glycosides [48]

)eobroma cacao L.            Alkaloids,
(Sterculiaceae);           anthraquinones,
60,111/HNC               cardiac glycosides,
                          and saponins [50]

Uapaca guineensis             Steroids,
Muell. Arg.                   alkaloid,
(Euphorbiaceae);           terpenoids, and
53,136/HNC                 gallic acid [53]

Species (family);         Known antimicrobial
voucher                      activities of
number                           plants

Azadirachta             Antibacterial activity
indica A. Juss         of ethanol leaf extract:
(Meliaceae);             Ec, Kp, Pm, Sa, Pa, Ef
4447/SRFK                  [18]; ethanol and
                          methanol extract of
                          leaves: Ec, Pa, St,
                              Sa, Bp [17]

Citrus grandis               Antibacterial
(L.) Osbeck                   activity of
(Rutaceae);                petroleum ether,
25,860/SRFC                  ethyl acetate,
                         chloroform, ethanol,
                            and leaf water:
                          Ec, Sa, Pa, Pm [21]

Cucurbita               Antibacterial activity
maxima Duch.                of aqueous seed
(Cucurbitaceae);         extract: Ec, Sa, Kp,
42,449/HNC               Ef, Pa [24], ethanol
                          and aqueous extract
                          of flowers: St, Ec,
                              Ef, Bc [26]

Dacryodes edulis             Antibacterial
(G. Don) H. J.                activity of
Lam (Burseraceae);         hydromethanolic,
1874/SRFK                  butanol, aqueous,
                          ethanolic extract,
                           ethyl acetate of
                             bark: Ec, Pa,
                              Bc, Sa [27]

Hibiscus                      Not reported
esculentus L.
(Malvaceae);
42,823/HNC

Ipomoea                       Not reported
batatas (L.) Lam
(Convolvulaceae);
55,594/HNC

Irvingia gabonensis          Antibacterial
(Aubry. Lec. ex O.        activity of aqueous
Rorke) Baill.             and ethanol extract
(Irvingiaceae);           of leaves and bark:
52,936/HNC               Sa, Ec [36]; S: Bst,
                         Ca, Cf, Ea, Ecl, Mm,
                          Ng, Pa, Pm, Pv, Sa,
                          Sd; Bc, Bm, Bs, Ck,
                           Ec, Kp, Sfl, St,
                                Sf [38]

Phaseolus                    Antibacterial
vulgaris                  activity of aqueous,
L. (Fabaceae);           alcohol, chloroform,
42,587/HNC                 ether extract of
                          seeds: Sa, Pa, Sf,
                            Bs, Kp, Ec [41]

Ricinodendron                Antibacterial
heudelotii (Baill.)           activity of
Pierre ex Heckel           methanol extract
(Euphorbiaceae);             of the leaves:
50,852/HNC                  Sa, Sf, Pv, Cf,
                          Mm, Ko, Kp, Ec, Pa,
                         St [43], Pf, Bs, Sa,
                            Ec, Ca, Af [44],
                            Ec, Ea, Pa, Ps,
                              Kp, Ecl [18]

Saccharum                    Antibacterial
officinarum L.                activity of
(Poaceae);                 methanol extract
42,958/HNC                 of the stems: Ec,
                            Kp, Sa, Pa [46]

Spondias                     Antibacterial
mombin L.                 activity of ethanol,
(Anacardiaceae);           methanol, water,
21,249/SRFK                   and acetone
                            extracts of the
                          leaves: Kp, Sa, St,
                              Ea, Sm [48]

)eobroma cacao L.            Antibacterial
(Sterculiaceae);             activity: Sa,
60,111/HNC                  Ec, Sd, Kp, Sm,
                              Pa, Pm [51]

Uapaca guineensis             Not reported
Muell. Arg.
(Euphorbiaceae);
53,136/HNC

HNC: Herbier National du Cameroun; SRFC: Societe des Reserves
Forestieres du Cameroun; SRFK: Societe des Reserves forestieres
du Kamerun; Af: Aspergillus flavus; Bp: Bacillus pumilus; Bc:
Bacillus cereus; Bm: Bacillus megaterium; Bs: Bacillus subtilis;
Ca: Candida albicans; Cf; Citrobacter freundii; Ck: Candida krusei;
Ea: Enterobacter aerogenes; Ec: Escherichia coli; Ecl: Enterobacter
cloacae; Ef: Enterococcus faecium; Kp: Klebsiella pneumoniae; Ko:
Klebsiella oxytoca; Mm: Morganella morganii; Ng: Neisseria
gonorrhoeae; Pa: Pseudomonas aeruginosa; Pf: Pseudomonas
fluorescens; Pm: Proteus mirabilis; Ps: Providencia stuartii; Pv:
Proteus vulgaris; Sa: Staphylococcus aureus; Sd: Shigella
dysenteriae; Sf; Streptococcus faecalis; Sf l: Shigella flexneri;
Sm: Serratia marcescens; St: Salmonella typhi.

Table 2: Bacterial strains and features.

Bacteria                         Features                References

ATCC 25923                   Reference strain                --
S. aureus MSSA1    Clinical isolate: Met susceptible;      [8, 9]
                         [Nis.sup.r], [Chl.sup.r]
S. aureus MRSA3      Clinical isolate: [Ofxa.sup.r],        [8]
                        [Kan.sup.r], [Tet.sup.r],
                               [Erm.sup.r]
S. aureus MRSA4      Clinical isolate: [Ofxa.sup.r],       [8, 9]
                        [Kan.sup.r], [Cyp.sup.r],
                        [Chl.sup.r], [Gen.sup.r],
                         [Nis.sup.r], [Amp.sup.r]
S. aureus MRSA6      Clinical isolate: [Ofxa.sup.r],       [8, 9]
                        [Flx.sup.r], [Kan.sup.r],
                        [Tet.sup.r], [Cyp.sup.r],
                       IM[/Cs.sup.r], [Chl.sup.r],
                        [Gen.sup.r], [Nis.sup.r],
                               [Amp.sup.r]
S. aureus MRSA8      Clinical isolate: [Ofxa.sup.r],       [8, 9]
                        [Flx.sup.r], [Kan.sup.r],
                        [Erm.sup.r], [Cyp.sup.r],
                       Im[/Cs.sup.r], [Chl.sup.r],
                        [Gen.sup.r], [Nis.sup.r],
                               [Amp.sup.r]
S. aureus MRSA9      Clinical isolate: [Ofxa.sup.r],       [8, 9]
                        [Flx.sup.r], [Tet.sup.r],
                        [Erm.sup.r], [Cyp.sup.r],
                       Im[/Cs.sup.r], [Chl.sup.r],
                        [Gen.sup.r], [Nis.sup.r],
                               [Amp.sup.r]
S. aureus MRSA11     Clinical isolate: [Ofxa.sup.r],       [8, 9]
                        [Kan.sup.r], [Erm.sup.r],
                       [Cyp.sup.r], Im[/Cs.sup.r],
                        [Chl.sup.r], [Nis.sup.r],
                               [Amp.sup.r]
S. aureus MRSA12     Clinical isolate: [Ofxa.sup.r],       [8, 9]
                        [Flx.sup.r], [Kan.sup.r],
                       [Erm.sup.r], Im[/Cs.sup.r],
                        [Chl.sup.r], [Gen.sup.r],
                         [Nis.sup.r], [Amp.sup.r]
SA01                 Clinical isolate: [Erm.sup.r],         [54]
                               [Amp.sup.r]
SA07                 Clinical isolate: [Erm.sup.r],         [54]
                               [Dox.sup.r]
SA18                 Clinical isolate: [Amp.sup.r],         [54]
                         [Dox.sup.r], [Vm.sup.r]
SA23                 Clinical isolate: [Imi.sup.r],         [54]
                               [Aug.sup.r]
SA36                 Clinical isolate: [Dox.sup.r],         [54]
                                [Vm.sup.r]
SA39                  Clinical isolate: [Amp.sup.r]         [54]
SA56                 Clinical isolate: [Amp.sup.r],         [54]
                               [Dox.sup.r]
SA64                 Clinical isolate: [Amp.sup.r],         [54]
                               [Dox.sup.r]
SA68                 Clinical isolate: [Amp.sup.r],         [54]
                                [Vm.sup.r]
SA88                 Clinical isolate: [Erm.sup.r],         [54]
                                [Vm.sup.r]
SA114                Clinical isolate: [Amp.sup.r],         [54]
                               [Dox.sup.r]
SA116                 Clinical isolate: [Erm.sup.r]         [54]
SA124                 Clinical isolate: [Erm.sup.r]         [54]
SA126                Clinical isolate: [Amp.sup.r],         [54]
                               [Dox.sup.r]
SA127                Clinical isolate: [Amp.sup.r],         [54]
                               [Dox.sup.r]
SA135                 Clinical isolate: [Erm.sup.r]         [54]
SA139                 Clinical isolate: [Erm.sup.r]         [54]

[Chl.sup.r], [Cyp.sup.r], [Erm.sup.r], [Flx.sup.r], Im[/Cs.sup.r],
[Kan.sup.r], Metr, [Ofxa.sup.r], [Tet.sup.r], [Vm.sup.r],
[Amp.sup.r], [Dox.sup.r], [Aug.sup.r], [Gen.sup.r], and [Nis.sup.r]
resistance to chloramphenicol, ciprofloxacin, e flomoxef,
imipenem/cilastatin sodium, kanamycin, methicillin, ofloxacin,
[Tet.sup.r]acycline, vancomycin, ampicillin, doxycycline, augmentin,
gentamicin, and nisin, respectively, SA: Staphylococcus aureus.

Table 3: Extraction yields and phytochemical composition of the
plant extracts.

Plant extract and part used     Yields   Alkaloids   Polyphenols
                                 (%)

Azadirachta indica      Bark     10.3        +            +
Citrus grandis         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         -            +
Ricinodendron           Bark     2.9         -            +
heudelotii             Leaves    7.2         -            +
Spondias mombin        Leaves    21.4        -            +
Saccharum              Leaves    8.4         -            +
officinarum
Theobroma cacao       Leaves     3.1         -            +
                       Beans     6.2         +            +
Uapaca guineensis     Leaves     7.3         -            +
                        Bark     6.1         +            +

Plant extract and part used     Flavonoids   Anthraquinones   Tannins

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

Plant extract and part used     Triterpenes   Steroids   Saponins

Azadirachta indica      Bark         -           +          +
Citrus grandis         Leaves        +           +          -
Cucurbita maxima       Beans         +           +          +
                       Leaves        +           +          +
Dacryodes edulis        Bark         +           +          +
                       Seeds         +           +          +
Hibiscus esculentus    Leaves        -           +          -
Ipomoea batatas        Beans         +           -          +
Irvingia gabonensis    Leaves        -           +          +
Phaseolus vulgaris     Leaves        -           +          +
Ricinodendron           Bark         +           +          -
heudelotii             Leaves        +           +          +
Spondias mombin        Leaves        +           +          -
Saccharum              Leaves        -           +          +
officinarum
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.

Table 4: MIC and MBC of the plant extracts and ciprofloxacin
against Staphylococcus aureus strains.

                  Samples (b), MIC and MBC in [micro]g/mL
                             (in parentheses)

                               Plant extracts

Bacterial
strains (a)       AIB         CGL         CMB          DES

ATCC 25923      1024 (-)       --          --        1024 (-)
SA01            512 (-)     1024 (-)       --        512 (-)
SA07            1024 (-)       --          --        512 (-)
SA18           512 (1024)   1024 (-)       --        512 (-)
SA23            1024 (-)    512 (-)        --        512 (-)
SA36            512 (-)        --       1024 (-)    256 (1024)
SA39            1024 (-)    1024 (-)       --        512 (-)
SA56            1024 (-)       --          --        1024 (-)
SA64            512 (-)     512 (-)     1024 (-)     512 (-)
SA68            1024 (-)       --          --        1024 (-)
SA88            512 (-)     1024 (-)    1024 (-)     512 (-)
SA114           1024 (-)       --          --        1024 (-)
SA116              --       1024 (-)       --        512 (-)
SA124              --       1024 (-)       --        512 (-)
SA126           1024 (-)       --       1024 (-)     512 (-)
SA127           512 (-)        --          --        1024 (-)
SA135           1024 (-)       --          --       512 (1024)
SA139           512 (-)        --          --        512 (-)
MSSA1           512 (-)        --      256 (512)    512 (1024)
MRSA3          512 (1024)   1024 (-)    256 (-)     512 (1024)
MRSA4           512 (-)     512 (-)     64 (512)    512 (512)
MRSA6           512 (-)     512 (-)       128        512 (-)
MRSA8           512 (-)     1024 (-)   128 (1024)    256 (-)
MRSA9           512 (-)     1024 (-)      128        512 (-)
MRSA 11         1024 (-)    1024 (-)      256        512 (-)
MRSA12          512 (-)     1024 (-)      128        512 (-)

                  Samples (b), MIC and MBC in [micro]g/mL
                             (in parentheses)

                               Plant extracts

Bacterial
strains (a)       DEB         DEL         HEL         IBL

ATCC 25923      512 (-)     1024 (-)       --          --
SA01            512 (-)     512 (-)     512 (-)        --
SA07            512 (-)     512 (-)     512 (-)     1024 (-)
SA18            512 (-)     512 (-)     512 (-)        --
SA23            512 (-)     1024 (-)    512 (-)     1024 (-)
SA36            1024 (-)    1024 (-)    512 (-)     1024 (-)
SA39            1024 (-)    1024 (-)    1024 (-)       --
SA56            1024 (-)    1024 (-)    1024 (-)       --
SA64            1024 (-)    512 (-)     512 (-)     1024 (-)
SA68            1024 (-)    1024 (-)    1024 (-)    1024 (-)
SA88            1024 (-)    1024 (-)    512 (-)     1024 (-)
SA114           1024 (-)    1024 (-)    256 (-)     512 (-)
SA116           1024 (-)    512 (-)     512 (-)        --
SA124           1024 (-)       --          --       1024 (-)
SA126           512 (-)     1024 (-)    512 (-)     1024 (-)
SA127           1024 (-)    1024 (-)    512 (-)     1024 (-)
SA135           1024 (-)    1024 (-)    1024 (-)       --
SA139           512 (-)        --       1024 (-)    1024 (-)
MSSA1           1024 (-)    256 (-)    512 (1024)   1024 (-)
MRSA3           1024 (-)    512 (-)     1024 (-)       --
MRSA4          512 (1024)   256 (-)     1024 (-)    1024 (-)
MRSA6           1024 (-)    1024 (-)       --       512 (-)
MRSA8           256 (-)     512 (-)    512 (1024)      --
MRSA9           512 (-)     1024 (-)    512 (-)     256 (-)
MRSA 11         512 (-)     1024 (-)    512 (-)     1024 (-)
MRSA12          256 (-)     256 (-)     512 (-)        --

                  Samples (b), MIC and MBC in [micro]g/mL
                             (in parentheses)

                               Plant extracts

Bacterial
strains (a)      IGB         PVL          RHB          RHL

ATCC 25923        --       512 (-)      1024 (-)     512 (-)
SA01              --       512 (-)         --        512 (-)
SA07              --       1024 (-)        --        512 (-)
SA18           1024 (-)    512 (-)      1024 (-)     512 (-)
SA23           1024 (-)    512 (-)      1024 (-)     512 (-)
SA36              --       1024 (-)     512 (-)      512 (-)
SA39              --       1024 (-)     1024 (-)        --
SA56           1024 (-)    512 (-)         --        512 (-)
SA64              --       512 (-)      256 (-)      1024 (-)
SA68              --       1024 (-)     1024 (-)     512 (-)
SA88              --      512 (1024)       --        512 (-)
SA114             --       512 (-)      512 (-)         --
SA116          1024 (-)    1024 (-)        --        1024 (-)
SA124             --          --           --        1024 (-)
SA126             --       1024 (-)     1024 (-)     1024 (-)
SA127             --      512 (1024)       --        1024 (-)
SA135             --       1024 (-)        --        512 (-)
SA139             --       512 (-)      1024 (-)     512 (-)
MSSA1             --       512 (-)     256 (1024)   512 (1024)
MRSA3          1024 (-)    512 (-)      256 (-)      1024 (-)
MRSA4             --       128 (-)      128 (-)      1024 (-)
MRSA6             --       1024 (-)     256 (-)      256 (-)
MRSA8             --       512 (-)      256 (-)      512 (-)
MRSA9          1024 (-)    512 (-)      256 (-)      512 (-)
MRSA 11        1024 (-)    512 (-)      256 (-)      512 (-)
MRSA12            --       1024 (-)     256 (-)      512 (-)

                  Samples (b), MIC and MBC in [micro]g/mL
                             (in parentheses)

                               Plant extracts

Bacterial
strains (a)      SML        SOL        TCB        TCL         UGL

ATCC 25923        --      1024 (-)      --         --          --
SA01              --      1024 (-)   512 (-)       --       512 (-)
SA07              --      1024 (-)      --         --       512 (-)
SA18              --      512 (-)    512 (-)       --       512 (-)
SA23           1024 (-)   1024 (-)   512 (-)    512 (-)     512 (-)
SA36           1024 (-)   1024 (-)   1024 (-)      --       512 (-)
SA39           1024 (-)      --         --      512 (-)     512 (-)
SA56              --      1024 (-)      --         --          --
SA64           1024 (-)      --         --      1024 (-)    512 (-)
SA68              --         --      1024 (-)      --          --
SA88              --      1024 (-)   1024 (-)   1024 (-)    1024 (-)
SA114          1024 (-)   1024 (-)      --      512 (-)     512 (-)
SA116          1024 (-)   1024 (-)      --         --       512 (-)
SA124             --         --         --      512 (-)        --
SA126             --         --         --      1024 (-)    1024 (-)
SA127          1024 (-)      --         --         --          --
SA135             --      1024 (-)      --         --          --
SA139             --      1024 (-)      --      1024 (-)       --
MSSA1             --      1024 (-)   256 (-)    512 (-)    266 (1024)
MRSA3          512 (-)       --      256 (-)    256 (-)     256 (-)
MRSA4          1024 (-)   1024 (-)   256 (-)    512 (-)     256 (-)
MRSA6             --         --      128 (-)    256 (-)     256 (-)
MRSA8             --      512 (-)    128 (-)    512 (-)     256 (-)
MRSA9          256 (-)    512 (-)    128 (-)    512 (-)     128 (-)
MRSA 11           --         --      128 (-)    512 (-)     256 (-)
MRSA12            --      1024 (-)   128 (-)    512 (-)     256 (-)

                Samples (b), MIC and
                MBC in [micro]g/mL
                 (in parentheses)

                  Plant
                 extracts

Bacterial                   Antibiotic
strains (a)       UGB           CIP

ATCC 25923         --        <0.5 (16)
SA01            512 (-)      <0.5 (4)
SA07               --        <0.5 (1)
SA18            1024 (-)     <0.5 (8)
SA23            512 (-)        <0.5
SA36            512 (-)        1 (8)
SA39            512 (-)      <0.5 (16)
SA56            1024 (-)     <0.5 (4)
SA64            1024 (-)       4 (8)
SA68               --          <0.5
SA88            1024 (-)     <0.5 (2)
SA114           512 (-)     <0.5 (<0.5)
SA116              --       <0.5 (<0.5)
SA124              --       <0.5 (<0.5)
SA126              --       <0.5 (<0.5)
SA127              --       <0.5 (<0.5)
SA135              --        <0.5 (1)
SA139           1024 (-)    <0.5 (<0.5)
MSSA1          128 (1024)     2 (16)
MRSA3           128 (-)       2 (16)
MRSA4           256 (-)       1 (16)
MRSA6           128 (-)        2 (8)
MRSA8           128 (-)        2 (8)
MRSA9            64 (-)       2 (16)
MRSA 11         128 (-)       2 (16)
MRSA12          128 (-)        2 (4)

(a) Bacterial strain (SA: Staphylococcus aureus; MRSA:
methicillin-resistant Staphylococcus aureus), (b) samples
(AIB: Azadirachta indica bark, CGL: Citrus grandis, CMB:
Cucurhita maxima beans, DES: Dacryodes edulis seeds, DEB:
Dacryodes edulis bark, DEL: Dacryodes edulis leaves, HEL:
Hibiscus esculentus leaves, IBL: Ipomoea batatas leaves,
IGB: Irvingia gabonensis beans, PVL: Phaseolus vulgaris
leaves, RHL: Ricinodendron heudelotii leaves, RHB:
Ricinodendron heudelotii bark, SML: Spondias mombin leaves,
SOL: Saccharum officinarum leaves, TCB: Theobroma cacao
beans, TCL: Theobroma cacao leaves, UGL: Uapaca guineensis
leaves, UGB: Uapacaguineensis bark, and CIP: ciprofloxacin);
R: MBC/MIC; (-): > 1024(MIC); nc, not calculated; MIC:
minimal inhibitory concentration; MBC: minimal bactericidal
concentration; CIP: ciprofloxacin; --: MIC and MBC at up to
1024 [micro]g/mL; MIC in bold: significant activity
[37, 60].

Table 5: MIC of extracts and ciprofloxacin in the absence (-)
and presence (+) of carbonyl cyanide m-chlorophenyl hydrazone (CCCP)
against selected strains of Staphylococcus aureus.

                   Samples (b) and MIC in [micro]g/mL and fold
                      increase of activity (in parentheses)

                   DES                 HEL               UGB
Bacterial
strains (a)    -         +         -        +        -         +

ATCC 25923    256     32 (32)#    256   <8 (>32)#    --    <8 (>128)#
MRSA3         256    <8 (>32)#    256   <8 (>32)#   512    <8 (>64)#
MRSA4         256     16 (16)#    128    16 (8)#    1024    128 (8)#
MRSA6         128    <8 (>16)#    256   <8 (>32)#   1024   <8 (>128)#
MRSA8         256     128 (2)#    128    128 (1)     --    512 (>2)#
MRSA9         128    <8 (>16)#    64    <8 (>8)#    1024   <8 (>128)#
MRSA11        256    <8 (>32)#    128   <8 (>16)#   1024   <8 (>128)#
MRSA12        256    <8 (>32)#    128   <8 (>16)#   1024   <8 (>128)#
SA01          128    <8 (>16)#    128   <8 (>16)#   1024   <8 (>128)#
SA07          512    <8 (>64)#    512    512 (1)    512     512 (1)
SA18          1024    128 (8)#    256   128 (2)#    1024    512 (2)#
SA88          512     512 (1)     --       --       1024    1024 (1)
SA114         1024   <8 (>128)#   --       --       1024    128 (8)#
SA135         512     64 (8)#     --       --        --    128 (>8)#

               Samples (b) and MIC in [micro]g/mL
                 and fold increase of activity
                       (in parentheses)

                   UGL                CIP
Bacterial
strains (a)    -         +         -        +

ATCC 25923    1024   <8 (>128)#    2     1 (2)#
MRSA3         512    <8 (>64)#     1   <0.5 (>2)#
MRSA4         1024    64 (16)#     2   <0.5 (>4)#
MRSA6         512    <8 (>64)#     1   <0.5 (>2)#
MRSA8         512    128 (>4)#   <0.5   <0.5 (nd)
MRSA9         256    <8 (>32)#   <0.5   <0.5 (nd)
MRSA11        256    <8 (>32)#     1      1(1)
MRSA12        256    <8 (>32)#   <0.5   <0.5 (nd)
SA01          256    <8 (>32)#   <0.5   <0.5 (nd)
SA07          256    <8 (>32)#   <0.5   <0.5 (nd)
SA18          512    <8 (>64)#     1   <0.5 (>2)#
SA88          1024   256 (>4)#     1   <0.5 (>2)#
SA114         512    <8 (>64)#   <0.5  <0.5 (>2)#
SA135         512    <8 (>64)#     1   <0.5 (>2)#

(a) Bacterial strain (SA: Staphylococcus aureus; MRSA: methicillin-
resistant Staphylococcus aureus), (b) samples (DES: Dacryodes
edulis seeds, HEL: Hibiscus esculentus leaves, UGL: Uapacaguineensis
leaves, UGB: Uapacaguineensis bark, and CIP: ciprofloxacin);
MIC: minimal inhibitory concentration; CCCP was tested at 0.5
[micro]g/mL; (-): >1024 [micro]g/mL; values in # represent increase
of activity [greater than or equal to] 2.

Table 6: MIC of extracts and ciprofloxacin in the absence (-) and
presence (+) of chlorpromazine (CPZ) against selected strains of
Staphylococcus aureus.

                 Samples (b) and MIC in [micro]g/mL and fold
                    increase of activity (in parentheses)

                   DES               HEL              UGB
Bacterial
strains (a)    -        +        -        +        -        +

ATCC 25923    512    512 (1)     --       --      512    512 (1)
MRSA3         256    256 (1)    1024   1024 (1)   512    512 (1)
MRSA4         512    512 (1)     --       --      256    256 (1)
MRSA6         256    256 (1)    512    128 (2)    512    512 (1)
MRSA8         256    256 (1)    1024   1024 (1)   256    256 (1)
MRSA9         256    256 (1)    1024   1024 (1)   512    512 (1)
MRSA11        512    512 (1)    1024   1024 (1)   512    512 (1)
MRSA12        512    512 (1)     --       --      512    512 (1)
SA01          512    512 (1)    1024   1024 (1)   512    512 (1)
SA07          512    512 (1)    1024   1024 (1)   512    512 (1)
SA18          512    512 (1)     --       --      1024   1024 (1)
SA88          512    512 (1)     --       --      1024   1024 (1)
SA114         1024   1024 (1)    --       --      1024   1024 (1)
SA135         512    512 (1)     --       --      1024   1024 (1)

                 Samples (b) and MIC in
                 [micro]g/mL and fold
                 increase of activity
                   (in parentheses)

                    UGL                CIP
Bacterial
strains (a)    -          +         -       +

ATCC 25923    128    1024 (0.13)    2     2 (1)
MRSA3          --        --         4     4(1)
MRSA4         1024    1024 (1)      2     2 (1)
MRSA6         256      -(0.25)      2     2 (1)
MRSA8          --        --         1    2 (0.5)
MRSA9         256      -(0.25)      1    2 (0.5)
MRSA11        128     -(<0.13)      4     4 (1)
MRSA12         --        --         2     2 (1)
SA01          512      512 (1)      1     1 (1)
SA07          1024    1024 (1)      4     4 (1)
SA18           --        --         1     1 (1)
SA88           --        --         4     4 (1)
SA114          --        --         1     1 (1)
SA135          --        --         1     1 (1)

(a) Bacterial strain (SA: Staphylococcus aureus; MRSA:
methicillin-resistant Staphylococcus aureus); (b) samples
(DES: Dacryodes edulis seeds, HEL: Hibiscus esculentus
leaves, UGL: Uapaca guineensis leaves, UGB: Uapaca
guineensis bark, CIP: ciprofloxacin); CPZ: chlorpromazine
at 25 [micro]g/mL; CIP: ciprofloxacin; MIC: minimal
inhibitory concentration.
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Title Annotation:Research Article
Author:Wamba, Brice E.N.; Mbaveng, Armelle T.; Nayim, Paul; Dzotam, Joachim K.; Ngalani, Ornella J.T.; Kuet
Publication:International Journal of Microbiology
Date:Jan 1, 2018
Words:9340
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