Printer Friendly

Tristemma hirtum and Five Other Cameroonian Edible Plants with Weak or No Antibacterial Effects Modulate the Activities of Antibiotics against Gram-Negative Multidrug-Resistant Phenotypes.

1. Introduction

During the last decade, the number of multidrug-resistant (MDR) pathogenic bacteria has dramatically increased all over the world [1-3]. The burden of MDR Gram-negative bacteria infections is particularly concerning because such bacteria are demonstrating resistance to nearly all currently licensed antibiotics [2, 4]. As a consequence, inadequate empirical antibacterial therapy of severe infections caused by MDR Enterobacteriaceae as well as Pseudomonas aeruginosa and Acinetobacter baumannii has been associated with increased morbidity and mortality [5, 6]. In this alarming scenario, the discovery of novel drugs that could provide clinical efficacy against MDR Gram-negative pathogens remains one of the keys to successfully overcome the tide of resistance [1, 4]. Targeting MDR systems as efflux in antibiotic resistant pathogens seems to be one of the most important existing strategies [4, 7]. For example, the drug combination ceftolozane-tazobactam has shown in vitro activity against selected MDR Gram-negative pathogens, including P. aeruginosa [8]. This combination is effective due to the ability of ceftolozane to evade multiple resistance mechanisms including efflux pumps, reduced uptake through porin channels, and modification of penicillin-binding proteins [9]. In the same goal, many other studies have been done and some are ongoing. Plants constitute an undeniable source for the discovery of new antibacterials acting directly as bacterial growth inhibitors or as antibiotic modulators [10-12]. Previous works showed that edible plants have excellent antibacterial properties and could also act as antibiotic modulators [13-18]. In the continuous contribution to the fight against infections due to MDR bacteria, this study was aimed to investigate the in vitro antibacterial activity as well as the antibiotic modulating activities of leaves of Tristemma hirtum and five other Cameroonian edible plants against selected Gram-negative MDR phenotypes.

2. Methods

2.1. Plant Material and Extraction. Six edible plants were collected in Bapa (5[degrees]16'0" north, 10[degrees]20'0" east) and Dschang (5[degrees]27'0" north, 10[degrees]4'0" east), two localities in the West Region of Cameroon. Samples collected were leaves of Aframomum letestuanum Gagnep. (Zingiberaceae) and Tristemma hirtum P. Beauv. (Melastomataceae), leaves and stem of Aframomum alboviolaceum (Ridl.) K.Schum. (Zingiberaceae), Pericarps of Cucurbita pepo Linn. (Cucurbitaceae) and Raphia hookeri Mann & Wendl. (Arecaceae), and the stem of Physalis peruviana L. (Solanaceae). The identification of the plants was done 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 number 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. Six reference antibiotics (RA) purchased from Sigma-Aldrich (Saint-Quentin-Fallavier, France) were tested: ceftriaxone (CEF), chloramphenicol (CHL), ciprofloxacin (CIP), erythromycin (ERY), kanamycin (KAN), and tetracycline (TET); p-iodonitrotetrazolium chloride (INT) (Sigma-Aldrich) was used as bacterial growth revelator; dimethylsulfoxide (DMSO) was used to dissolve the plant extracts.

2.3. Bacteria, Culture Media, and Growth Conditions. The twenty strains of Gram-negative bacteria tested in this study were MDR isolates (laboratory collection) and reference strains (American Type Culture Collection) of Escherichia coli (ATCC8739, AG100A, AG100ATet, AG102, MC4100, and W3110), Enterobacter aerogenes (ATCC13048, CM64, EA27, EA289, and EA294), Klebsiella pneumoniae (ATCC11296, KP55, KP63, and K24), Pseudomonas aeruginosa (PA01 and PA124), and Providencia stuartii (NEA16, PS2636, and PS299645). The clinical strains were the laboratory collection from UMR-MD1, University of Marseille, France. The bacterial features are reported in Table S1 (see supplementary materials). The microorganisms were cultured overnight on Mueller-Hinton Agar (MHA) 24 h prior to any assay. The Mueller-Hinton Broth (MHB) was used as liquid culture medium for susceptibility tests.

2.4. Preliminary Phytochemical Screening. Potential classes of potential antibacterial phytochemicals such as alkaloids (Dragendorff's and Mayer's tests), terpenoids: sterols (Salkowski's test), saponins (foam test) and triterpenes (Liebermann-Burchard test), and phenolics: anthraquinones (Borntrager's test), flavonoids (aluminum chloride test), polyphenols (ferric chloride test), and tannins (gelatin test) (Table 2) were investigated according to the described phytochemical methods [19, 20].

2.5. Microbial Susceptibility Testing. The minimal inhibitory concentration (MIC) and minimum bactericidal concentration (MBC) determinations on bacteria were performed using the rapid INT colorimetric assay [21] with some modifications as previously described [16, 22]. Samples were dissolved in DMSO/MHB. The final concentration of DMSO was lower than 2.5%. The 2-fold dilutions of samples were made in 96-well microplates and the tested bacterial concentration was 1.5 x [10.sup.6] colony forming units (CFU)/mL. The microplates were incubated at 37[degrees]C for 18 h. All assays were in triplicate and were repeated thrice. Wells containing MHB, 100 [micro]L of inoculum, and DMSO to a final concentration of 2.5% served as negative control. Extracts and CHL were tested in the concentration ranges of 16-2048 [micro]g/mL and 2-256 [micro]g/mL, respectively. 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 [16, 22]. 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 a sample, which did not induce a color change after addition of INT as mentioned above [16, 22].

2.6. Antibiotic-Activity Modulation Assays. To evaluate the potentiating effect of the tested crude extracts, a preliminary assay was performed using the association of extracts at their various subinhibitory concentrations with antibiotics against one of a problematic bacterium, P. aeruginosa PA124. MIC/2 and MIC/4 of extracts were selected as the best subinhibitory concentrations [16, 23]. Samples were tested at various subinhibitory concentrations (MIC/2, MIC/4, MIC/8, and MIC/16). Results allowed selecting MIC/2 and MIC/4 as subinhibitory concentrations for further experiments on selected Gram-negative bacteria. Briefly, after serial dilution of antibiotic, extract was added to each well at its subinhibitory concentration and the bacterial inoculation was done; the MIC was further determined. Antibiotics were tested in the concentration ranges of 2-256 [micro]g/mL or 0.5-64 [micro]g/mL when it was necessary. 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 cut-off for biological significance of antibiotic-resistance modulating effects [24].

3. Results

3.1. Phytochemical Composition of Plant Extracts. The results of the qualitative phytochemical screening showed that each plant extract contains at least one of the secondary metabolites classes such as alkaloids, anthraquinones, flavonoids, phenols, saponins, tannins, steroids, and triterpenes. Polyphenols and steroids were present in all the extracts (Table 2).

3.2. Antibacterial Activity. Plant extracts were tested for their antibacterial activities on a panel of 20 Gram-negative bacteria. Results summarized in Table 3 showed that all extracts were active on at least one bacterial strain with MIC values ranging from 512 to 2048 [micro]g/mL. The extracts of Raphia hookeri pericarps (RHP), Tristemma hirtum leaves (THL), and Cucurbitapepo pericarps (CPP) were more active. They presented the lowest MIC value (512 [micro]g/mL) against E. coli ATCC8739 (RHP), E. coli AG100 (THL), E. coli MC4100 (CCP and THL), P. stuartii PS299645 (RHP, CCP, and THL), E aerogenes EA294 (RHP), and P aeruginosa PA01 (RHP). In general, MBC values recorded for the extracts were more than 2048 [micro]g/mL.

3.3. Antibiotic-Resistance Modulation Activity of Extracts. The antibacterial activities of six commonly used antibiotics were evaluated in absence/presence of the different plant extracts. The results of the prescreening of the tested plant extracts for their antibiotic-resistance modulating effects against P. aeruginosa PA124 (Table 4) allowed us to select 4 plant extracts (leaves extracts of T. hirtum, Aframomum letestuanum, Aframomum alboviolaceum, and the pericarps extract of Raphia hookeri) for the study of their modulating effects against selected MDR bacteria, these at the concentrations equivalent to the half and quarter of their MIC values. It was observed that some extracts selectively improved the antibacterial activities of the tested antibiotics by decreasing their MIC values at about 2 to 64 times (Tables 5-8). The most important effects were observed with leaves extracts of Tristemma hirtum which significantly improved the antibacterial activities of all the tested antibiotics against 70% (7/10) to 100% (10/10) of the MDR bacteria used for the study. The activities of CHL, KAN, and CIP were mostly improved (2 to 128 times) as well as MIC/2 compared to at MIC/4 values (Table 8). The pericarps extract of Raphia hookeri also showed significant antibiotic-potentiating activities in more than 70% (7/10) of the tested MDR bacteria. Its modulating effect was more important when it was associated with CHL, KAN, STP, ERY, and TET, mainly at the half of its MIC values (Table 7). The antibiotic-modulating effects of the other extracts (Aframomum letestuanum and Aframomum alboviolaceum) were not significant. They were observed on less than 50% of the tested MDR bacteria (Tables 5 and 6).

4. Discussion

4.1. Phytochemical Composition of Extracts. Plant secondary metabolites including flavonoids, phenols, terpenoids, steroids, saponins, and tannins are known for their antimicrobial activities [25-27]. In this study, phytochemical screening of the tested extracts indicated the presence of at least one of these metabolites in each extract (Table 2). Their presence in the studied extracts could therefore explain the observed activities. Also, terpenoids and phenolics were previously reported in Aframomum alboviolaceum [16], Cucurbita pepo [28, 29], Physalisperuviana [30], Raphia hookeri [31, 32], and Tristemma hirtum [33]. Their presence in the tested plant extract is in conformity with the previous phytochemical investigations.

4.2. Antibacterial Potential of Extracts. Based on the cut-off values indicating the antibacterial activity of plant extracts proposed by Kuete [34], many of the tested extracts, especially those from Tristemma hirtum leaves (THL), Raphia hookeri pericarps (RHP), and Cucurbita pepo pericarps (CPP) had weak (>512 [micro]g/mL) to no activity (MIC > 2048 [micro]g/mL) against the tested bacteria (Table 2). Previous studies have already demonstrated their in vitro antibacterial activities against many pathogenic microorganisms including bacteria. Oboh et al. [35] demonstrated the antibacterial properties of Raphia hookeri syrup against E. coli, P. aeruginosa, and S. aureus. According to these authors, the observed activity may be attributed to the presence of phenolic compounds including tannins, saponins, and flavonoids, which were also highlighted in the methanol extract used in this work. With regard to Tristemma hirtum, the studies carried out byNoumedem [36] previously demonstrated its antibacterial activity against selected sensitive bacterial strains including E. coli, P. aeruginosa, S. flexneri, K. pneumonia, S. typhi, S. paratyphi, and E. faecalis. Ahoua et al. [37] showed that a plant belonging to the same genus, Tristemma coronatum, presented inhibitory power against various bacterial strains. This is in accordance with the results obtained in this study. Noumedem et al. [17] showed that the methanol leaves extract of Cucurbita pepo has significant antibacterial activity against the bacterial strains used in this work. The difference of the activity may be due to the fact that different parts of the plants were used in the two studies. Even though the antibacterial activities of the tested plant extracts were in general moderate to low, if we consider the features of the bacteria used in this study (Table S1, supplementary materials) and the fact that the plants used are edible plants, some like the extract of leaves of Tristemma hirtum and extracts of pericarps of Raphia hookeri and Cucurbita pepo could be used to fight bacterial infections.

4.3. Antibiotic-Modulation Effects of Extracts. Infections due to MDR Gram-negative bacteria are particularly concerning as such bacteria are demonstrating resistance to practically all current licensed therapies [2, 4, 38]. Numerous ranges of novel approaches are under investigation as potential alternative treatments. Among them, the use of plant-derived substances to target different antibiotic resistance systems in the bacteria is considered as one of the best strategies [10, 39, 40]. In this study, nine methanol plant extracts were tested for their ability to modulate the activity of some common antibiotics. As the main results, it was observed that the activities of all tested antibiotics, especially those of CHL, KAN, CIP, and TET, were improved 2 to 128 times against more than 70% of the tested MDR bacteria in the presence of the extracts of leaves of Tristemma hirtum and pericarps of Raphia hookeri (Tables 7 and 8). According to some reviews, plant-derived substances can act in synergy with antibiotics by inhibiting bacterial efflux pumps, allowing an increase of the intracellular concentrations of the antibiotics [7, 41]. Thus, because the bacteria used in this work express efflux pumps as the main resistance mechanism (Table S1, supplementary materials), the results obtained herein suggest that the aforesaid extracts could contain efflux pumps inhibitors [42]. According to Okusa and Duez [39], such effects may be due to the presence of alkaloids, flavonoids, terpenoids, and tannins in those extracts. Additionally, the tested extracts presented some antagonist actions with the antibiotics. This could be due to negative interactions between the antibiotics and the compounds present in the tested extracts. Finally, the most active extracts, extracts of leaves of Tristemma hirtum and pericarps of Raphia hookeri, could be used to stimulate the renewed use of antibiotics with reduced effectiveness due to resistance.

5. Conclusion

With respect to the main findings of this work, the extracts of leaves of Tristemma hirtum and pericarps of Raffia hookeri appear as sources of substances that can be promising potentiating agents of antibiotics, even though they have moderate direct antibacterial action against the tested MDR bacteria.

https://doi.org/10.1155/2018/7651482

Conflicts of Interest

The authors declare that they have no conflicts of interest.

Authors' Contributions

Gaelle S. Nguenang, Hermione T. Manekeng, Paul Nayim, and Brice E. N. Wamba carried out the study; Armelle T. Mbaveng and Victor Kuete designed the experiments; Aime G. Fankam, 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.

Supplementary Materials

Table S1: Gram-negative bacteria used and their features and further details on the antibiotic-resistance profiles of tested Gram-negative bacteria. (Supplementary Materials)

References

[1] M. Bassetti, F. Ginocchio, M. Mikulska, L. Taramasso, and D. R. Giacobbe, "Will new antimicrobials overcome resistance among Gram-negatives?" Expert Review of Anti-infective Therapy, vol. 9, no. 10, pp. 909-922, 2011.

[2] Z.-Q. Xu, M. T. Flavin, and J. Flavin, "Combating multidrug-resistant Gram-negative bacterial infections," Expert Opinion on Investigational Drugs, vol. 23, no. 2, pp. 163-182, 2014.

[3] M. Bassetti, D. Pecori, and M. Peghin, "Multidrug-resistant Gram-negative bacteria-resistant infections: Epidemiology, clinical issues and therapeutic options," Italian Journal of Medicine, vol. 10, no. 4, pp. 364-375, 2016.

[4] R. Huwaitat, A. P. McCloskey, B. F. Gilmore, and G. Laverty, "Potential strategies for the eradication of multidrug-resistant Gram-negative bacterial infections," Future Microbiology, vol. 11, no. 7, pp. 955-972, 2016.

[5] B. J. Kamicker, M. T. Sweeney, F. Kaczmarek et al., "Bacteria efflux pomp inhibitors," Methods in molecular medicine, vol. 142, pp. 187-204, 2008.

[6] M. D. Zilberberg, A. F. Shorr, S. T. Micek, C. Vazquez-Guillamet, and M. H. Kollef, "Multi-drug resistance, inappropriate initial antibiotic therapy and mortality in Gram-negative severe sepsis and septic shock: a retrospective cohort study," Critical Care, vol. 18, no. 6, p. 596, 2014.

[7] M. Stavri, L. J. V. Piddock, and S. Gibbons, "Bacterial efflux pump inhibitors from natural sources," Journal of Antimicrobial Chemotherapy, vol. 59, no. 6, pp. 1247-1260, 2007.

[8] J. L. Liscio, M. V. Mahoney, and E. B. Hirsch, "Ceftolozane/tazobactam and ceftazidime/avibactam: Two novel [beta]-lactam/[beta]-lactamase inhibitor combination agents for the treatment of resistant Gram-negative bacterial infections," International Journal of Antimicrobial Agents, vol. 46, no. 3, pp. 266-271, 2015.

[9] G. G. Zhanel, P. Chung, H. Adam et al., "Ceftolozane/tazobactam: A novel cephalosporin/[beta]-lactamase inhibitor combination with activity against multidrug-resistant gram-negative bacilli," Drugs, vol. 74, no. 1, pp. 31-51, 2014.

[10] T. Sibanda and A. I. Okoh, "The challenges of overcoming antibiotic resistance: plant extracts as potential sources of antimicrobial and resistance modifying agents," African Journal of Biotechnology, vol. 6, no. 25, pp. 2886-2896, 2007.

[11] O. A. Aiyegoro and A. I. Okoh, "Use of bioactive plant products in combination with standard antibiotics: implications in antimicrobial chemotherapy," Journal of Medicinal Plants Research, vol. 3, no. 13, pp. 1147-1152, 2009.

[12] M. Saleem, M. Nazir, M. S. Ali et al., "Antimicrobial natural products: an update on future antibiotic drug candidates," Natural Product Reports, vol. 27, no. 2, pp. 238-254, 2010.

[13] A. G. Fankam, V. Kuete, I. K. Voukeng, J. R. Kuiate, and J.-M. Pages, "Antibacterial activities of selected Cameroonian spices and their synergistic effects with antibiotics against multidrug-resistant phenotypes," BMC Complementary and Alternative Medicine, vol. 11, article no. 104, 2011.

[14] S. T. Lacmata, V Kuete, J. P. Dzoyem et al., "Antibacterial activities of selected cameroonian plants and their synergistic effects with antibiotics against bacteria expressing MDR phenotypes," Evidence-Based Complementary and Alternative Medicine, vol. 2012, Article ID 623723, 11 pages, 2012.

[15] I. K. Voukeng, V Kuete, J. P. Dzoyem et al., "Antibacterial and antibiotic-potentiation activities of the methanol extract of some cameroonian spices against Gram-negative multi-drug resistant phenotypes," BMC Research Notes, vol. 5, article no. 299, 2012.

[16] D. E. Djeussi, J. A. K. Noumedem, J. A. Seukep et al., "Antibacterial activities of selected edible plants extracts against multidrug-resistant Gram-negative bacteria," BMC Complementary and Alternative Medicine, vol. 13, article no. 164, 2013.

[17] J. A. K. Noumedem, M. Mihasan, S. T. Lacmata, M. Stefan, J. R. Kuiate, and V. Kuete, "Antibacterial activities of the methanol extracts of ten Cameroonian vegetables against Gram-negative multidrug-resistant bacteria," BMC Complementary and Alternative Medicine, vol. 13, article no. 26, 2013.

[18] J. K. Dzotam and V. Kuete, "Antibacterial and Antibiotic-Modifying Activity of Methanol Extracts from Six Cameroonian Food Plants against Multidrug-Resistant Enteric Bacteria," BioMed Research International, vol. 2017, Article ID 1583510, 2017.

[19] J. B. Harbone, Phytochemical Methods: A Guide to Modern Techniques of Plant Analysis, Chapman and Hall Ltd, London, UK, 1973.

[20] V. Kuete, Medicinal Plant Research in Africa in: Pharmacology and Chemistry, Elsevier, Oxford, UK, 1st edition, 2013.

[21] J. N. Eloff, "A sensitive and quick microplate method to determine the minimal inhibitory concentration of plant extracts for bacteria," Planta Medica, vol. 64, no. 8, pp. 711-713, 1998.

[22] V. Kuete, G. F. Wabo, B. Ngameni et al., "Antimicrobial activity of the methanolic extract, fractions and compounds from the stem bark of Irvingia gabonensis (Ixonanthaceae)," Journal of Ethnopharmacology, vol. 114, no. 1, pp. 54-60, 2007.

[23] A. G. Fankam, J.-R. Kuiate, and V. Kuete, "Antibacterial and antibiotic resistance modulatory activities of leaves and bark extracts of Recinodindron heudelotii (Euphorbiaceae) against multidrug-resistant Gram-negative bacteria," BMC Complementary and Alternative Medicine, vol. 17, no. 1, article no. 168, 2017.

[24] J. Kovac, N. Gavaric, F. Bucar, and S. S. Mozina, "Antimicrobial and resistance modulatory activity of alpinia katsumadai seed phenolic extract, essential oil and post-distillation extract," ood Technology and Biotechnology, vol. 52, no. 2, pp. 248-254, 2014.

[25] M. M. Cowan, "Plant products as antimicrobial agents," Clinical Microbiology Reviews, vol. 12, no. 4, pp. 564-582, 1999.

[26] J. L. Rios and M. C. Recio, "Medicinal plants and antimicrobial activity," Journal of Ethnopharmacology, vol. 100, no. 1-2, pp. 8084, 2005.

[27] K. L. Compean and R. A. Ynalvez, "Antimicrobial activity of plant secondary metabolites: A review," Research Journal of Medicinal Plant, vol. 8, no. 5, pp. 204-213, 2014.

[28] B.-. Carbin, B. Larsson, and O. Lindahl, "Treatment of Benign Prostatic Hyperplasia with Phytosterols," British Journal of Urology, vol. 66, no. 6, pp. 639-641, 1990.

[29] T. Karpagam, B. Varalakshmi, J. S. Bai, and S. Gomathi, "Effect of different doses of Cucurbita pepo linn extract as an anti-Inflammatory and analgesic nutraceautical agent on inflamed rats," International journal of periodontics & restorative dentistry, vol. 3, no. 3, pp. 184-192, 2011.

[30] M. F. Ramadan and J.-T. Morsel, "Oil goldenberry (Physalis peruviana L.)," Journal of Agricultural and Food Chemistry, vol. 51, no. 4, pp. 969-974, 2003.

[31] C. O. Ibegbulem, C. S. Alisi, P. Nwankpa, B. A. Amadi, M. A. Agiang, and V. S. Ekam, "Medicinal values of Elaeis guineensisand Raphia hookeriwines," Journal of Research in Biology, vol. 2, no. 6, pp. 589-595, 2012.

[32] M. N. Ogbuagu, "Vitamins, phytochemicals and toxic elements in the pulp and seed of raphia palm fruit (Raphia hookeri)," Fruits, vol. 63, no. 5, pp. 297-302, 2008.

[33] M. R. C. Dongmo, Evaluation of antidermatophytic activity of methanol extracts and fractions of Acalypha manniana (Euphorbiaceae) and Tristemma hirtum (Melastomataceae) [M.S. thesis], Department of Biochemistry, University of Dschang, Dschang, Cameroon, 2009.

[34] V. Kuete, "Potential of Cameroonian plants and derived products against microbial infections: A review," Planta Medica, vol. 76, no. 14, pp. 1479-1491, 2010.

[35] O. F. Oboh, L. Iyare, M. Idemudia, and S. Enabulele, "Physicochemical and nutritional characteristics, and antimicrobial activity of oil palm syrup, raffia palm syrup and honey," IOSR Journal of Pharmacy and Biological Sciences, vol. 11, no. 1, pp. 73-78, 2016.

[36] J. A. K. Noumedem, Antimicrobial, antioxidant and ant-diarrhea properties of Acalypha manniana and Tristemma hirtum [M.s. thesis], Department of Biochemistry, University of Dschang, Dschang, Cameroon, 2009.

[37] A. R. C. Ahoua, A. G. Konan, B. Bonfoh, and M. W. Kone, "Antimicrobial potential of 27 plants consumed by chimpanzees (Pan troglodytes verus Blumenbach) in Ivory Coast," BMC Complementary and Alternative Medicine, vol. 15, no. 1, article no. 383, 2015.

[38] M. T. Mascellino, M. D. Angelis, and A. Oliva, "Multi-drug resistant gram-negative bacteria: antibiotic-resistance and new treatment strategies," Diagnostic Pathology: Open Access, vol. 2, no. 2, 4 pages, 2017.

[39] P. N. Okusa and P. Duez, "Chapitre 13: Medicinal plants: a tool to overcome antibiotic resistance?" in Medicinal Plants: Classification, Biosynthesis and Pharmacology, A. Varela and J. Ibanez, Eds., pp. 315-330, Nova Science Publishers, Inc, New York, NY, USA, 2009.

[40] E. F. F. Matias, K. K. A. Santos, T. S. Almeida, J. G. M. Costa, and H. D. M. Coutinho, "Enhancement of antibiotic activity by Cordia verbenacea DC," Latin American Journal of Pharmacy, vol. 29, no. 6, pp. 1049-1052, 2010.

[41] G. Tegos, F. R. Stermitz, O. Lomovskaya, and K. Lewis, "Multidrug pump inhibitors uncover remarkable activity of plant antimicrobials," Antimicrobial Agents and Chemotherapy, vol. 46, no. 10, pp. 3133-3141, 2002.

[42] L. C. Braga, A. A. M. Leite, K. G. S. Xavier et al., "Synergic interaction between pomegranate extract and antibiotics against Staphylococcus aureus," Canadian Journal of Microbiology, vol. 51, no. 7, pp. 541-547, 2005.

[43] P. M. Abreu and R. G. Noronha, "Volatile constituents of the rhizomes of Aframomum alboviolaceum (Ridley) K. Schum. from Guinea-Bissan," Flavour and Fragrance Journal, vol. 12, no. 2, pp. 79-83, 1997.

[44] G. B. Ilumbe, P. Van Damme, F. L. Lukoki, V. Joiris, M. Visser, and J. Lejoly, "Contribution a letude des plantes medicinales dans le traitement des hemorroides par les pygmees Twa et leur voisin Oto de Bikoro, en RDC," Congo Sciences, vol. 2, no. 1, pp. 46-54, 2014.

[45] W. M. Kone, K. K. Atindehou, T. Dossahoua, and B. Betschart, "Anthelmintic activity of medicinal plants used in northern Cote d'Ivoire against intestinal helminthiasis," Pharmaceutical Biology, vol. 43, no. 1, pp. 72-78, 2005.

[46] D. M. Yemele, B. P. Telefo, S. C. Goka et al., "In vtro cytotoxicity studies of sixteen plants used for pregnant women's health conditions in menoua division-West Cameroon," International Journal of Phytomedicine, vol. 7, no. 2, pp. 235-239, 2015.

[47] G. K. A. Adepoju and A. A. Adebanjo, "Effect of consumption of Cucurbita pepo seeds on haematological and biochemical parameters," African Journal of Pharmacy and Pharmacology, vol. 5, no. 1, pp. 18-22, 2011.

[48] A. Jafarian, B. Zolfaghari, and M. Parnianifard, "The effects of methanolic, chloroform, and ethylacetate extracts of the cucurbita pepo L. On the delay type hypersensitivity and antibody production," Research in Pharmaceutical Sciences, vol. 7, no. 4, pp. 217-224, 2012.

[49] S. Sarkar and D. Guha, "Effect of ripe fruit pulp extract of Cucurbita pepo Linn. in aspirin induced gastric and duodenal ulcer in rats," Indian Journal of Experimental Biology (IJEB), vol. 46, no. 9, pp. 639-645, 2008.

[50] O. Cakir, M. Pekmez, E. Cepni, B. Candar, and K. Fidan, "Evaluation of biological activities of physalis peruviana ethanol extracts and expression of Bcl-2 genes in HeLa cells," Food Science and Technology, vol. 34, no. 2, pp. 422-430, 2014.

[51] M. B. Cueva, R. A. Tigre Leon, M. M. Angel Yanchaliquin, and I. F. Herminia Sanaguano Salguero, "Antibacterial Effects of Uvilla (Physalis peruviana L.) extracts against Listeria spp. Isolated from Meat in Ecuador," International Journal of Current Microbiology and Applied Sciences, vol. 6, no. 4, pp. 1146-1153, 2017.

[52] R. Irvine, Woody Plant of Ghana with Special Reference to Their Uses, Oxford University Press, Oxford, UK, 1961.

Gaelle S. Nguenang, Armelle T. Mbaveng (iD), Aime G. Fankam, Hermione T. Manekeng, Paul Nayim, Brice E. N. Wamba, and Victor Kuete (iD)

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

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

Received 17 December 2017; Revised 10 January 2018; Accepted 19 February 2018; Published 22 March 2018

Academic Editor: Carlos Henrique Gomes Martins
Table 1: Information on the studied plants.

Species (family);            Traditional uses
voucher number

Aframomum                   Against bacterial
alboviolaceum            infections, hemorrhoid,
(Ridl.) K.Schum.            and fever and as
(Zingiberaceae);          diuretic [16, 43, 44]
34888/HNC

Aframomum                  Against hemorrhage,
letestuanum              muscular pains, nausea,
Gagnep.                     and vomiting [46]
(Zingiberaceae);
43134/HNC

Cucurbita pepo Linn.      Against stomachache,
(Cucurbitaceae);          for hepatoprotection,
42512/HNC                     antidiabetic,
                           antimicrobial, and
                            anti-inflammatory
                          hypertension [47-49].

Physalis peruviana           Against asthma,
L. (Solanaceae);           hepatitis, malaria,
16547/SRF-Cam              and rheumatism [46]

Raphia hookeri           As laxative and against
Mann & Wendl.             malaria, measles, and
(Arecaceae);               infections [31, 52]
38372/HNC

Tristemma hirtum         Against typhoid fever,
R Beauv.                hemorrhoids, infertility,
(Melastomataceae);       and skin diseases [33].
33936/HNC

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

Aframomum                Alkaloids, flavonoids,
alboviolaceum            phenols, triterpenes,
(Ridl.) K.Schum.          and anthocyanin [16]
(Zingiberaceae);
34888/HNC

Aframomum                     Not reported
letestuanum
Gagnep.
(Zingiberaceae);
43134/HNC

Cucurbita pepo Linn.     Carotenoids, saponins,
(Cucurbitaceae);           tannins, quinones,
42512/HNC                 coumarins, lignins,
                         and alkaloids [28, 29]

Physalis peruviana          Polyphenols and
L. (Solanaceae);              steroids [30]
16547/SRF-Cam

Raphia hookeri           Alkaloids, flavonoids,
Mann & Wendl.            phenols, tannins, and
(Arecaceae);               saponins [31, 32].
38372/HNC

Tristemma hirtum         Alkaloids, flavonoids,
R Beauv.                 polyphenols, steroids,
(Melastomataceae);       tannins, saponins, and
33936/HNC                   triterpenes [33]

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

Aframomum                  Methanol extract of
alboviolaceum                rhizome against
(Ridl.) K.Schum.         Enterobacter aerogenes,
(Zingiberaceae);         Klebsiella pneumoniae,
34888/HNC                 Enterobacter cloacae
                          [16], and Haemonchus
                              contortus [45]

Aframomum                      Not reported
letestuanum
Gagnep.
(Zingiberaceae);
43134/HNC

Cucurbita pepo Linn.       Ethanol extract of
(Cucurbitaceae);             leaves against
42512/HNC                   Escherichia coli,
                         Klebsiella pneumoniae,
                             and providencia
                              stuartii [17]

Physalis peruviana         Ethanol extract of
L. (Solanaceae);        seeds against Lactococcus
16547/SRF-Cam             lactis [50], ethanol
                            extract and water
                          extract of leaves and
                        berries against Listeria
                                spp. [51]

Raphia hookeri           Effects of wine against
Mann & Wendl.               Escherichia coli,
(Arecaceae);             Pseudomonas aeruginosa,
38372/HNC                 Bacillus cereus, and
                             Staphylococcus
                             aureus [31, 35]

Tristemma hirtum               Not reported
R Beauv.
(Melastomataceae);
33936/HNC

HNC: Herbier National du Cameroun; SRF-Cam: Societe des
Reserves Forestieres du Cameroun.

Table 2: Extraction yields and phytochemical composition
of the plant extracts.

Plant extracts            Part used   Yields (%)   alk   pol   flav

Aframomum alboviolaceum      Stem        3.1        +     +     +
                            Leaves       8.7        +     +     +
Aframomum letestuanum       Leaves       3.7        +     +     +
Cucurbita pepo            Pericarps      9.1        +     +     +
Physalis peruviana           Stem        4.05       +     +     -
Raphia hookeri            Pericarps      5.2        +     +     +
Tristemma hirtum            Leaves       10.4       -     +     +

Plant extracts             anthr   tan   tri   ster   sap

Aframomum alboviolaceum      +      +     +     +      -
                             +      -     +     +      +
Aframomum letestuanum        -      +     +     +      +
Cucurbita pepo               -      +     +     +      -
Physalis peruviana           +      +     +     +      -
Raphia hookeri               +      +     -     +      +
Tristemma hirtum             +      -     +     +      +

-: absent; +: present. Yield was calculated as the ratio of the
mass of the obtained methanol extract/mass of the plant powder.
alk: alkaloids; anthr: anthraquinones; flav: flavonoids; pol:
polyphenols; sap: saponins; ster: steroids; tan: tannins;
tri: triterpenes.

Table 3: Minimal inhibitory concentrations (MIC) and minimal
bactericidal concentrations (MBC) of the plant extracts
and chloramphenicol against bacteria strains.

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

                                      Plant extracts

Bacterial strains (a)         AAS           AAL           ALL

Escherichia coli
ATCC8739                   2048 (-)      2048 (-)      2048 (-)
AG100A                    1024 (2048)    1024 (-)        1024
AG100ATET                  2048 (-)      1024 (-)     1024 (1024)
AGI 02                        --            --            --
W3110                      1024 (-)      1024 (-)     1024 (1024)
MC4100                     1024 (-)      1024 (-)      1024 (-)
Enterobacter aerogenes
ATCC13048                  1024 (-)      1024 (-)      1024 (-)
EA289                         --            --            --
EA294                     1024 (2048)   1024 (2048)   1024 (2048)
EA27                         2048           --            --
CM64                          --            --            --
Klebsiella pneumoniae
ATCC11296                     --         1024 (-)      1024 (-)
KP55                       1024 (-)      1024 (-)      1024 (-)
KP63                          --            --            --
K24                           --         1024 (-)      1024 (-)
Providencia stuartii
PS299645                   2048 (-)      1024 (-)      1024 (-)
NEA16                         --            --            --
PS2636                        --            --            --
Pseudomonas aeruginosa
PA01                          --         1024 (-)      1024 (-)
PA124                         --            --            --

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

                                       Plant extracts

Bacterial strains (a)       CCP        PPS          RHP         THL

Escherichia coli
ATCC8739                  2048 (-)   2048 (-)   512 (1024)    2048 (-)
AG100A                    512 (-)    2048 (-)   512 (1024)    512 (-)
AG100ATET                    --      2048 (-)    1024 (-)        --
AGI 02                       --         --          --           --
W3110                     1024 (-)      --      1024 (2048)   1024 (-)
MC4100                    512 (-)    2048 (-)    1024 (-)     512 (-)
Enterobacter aerogenes
ATCC13048                 2048 (-)   2048 (-)    1024 (-)     2048 (-)
EA289                     2048 (-)      --          --        2048 (-)
EA294                     2048 (-)      --        512 (-)     2048 (-)
EA27                      2048 (-)      --          --        2048 (-)
CM64                         --         --          --           --
Klebsiella pneumoniae
ATCC11296                 1024 (-)      --          --        1024 (-)
KP55                      1024 (-)      --        512 (-)     1024 (-)
KP63                         --         --          --           --
K24                          --         --       2048 (-)        --
Providencia stuartii
PS299645                  512 (-)    2048 (-)     512 (-)     512 (-)
NEA16                     2048 (-)      --          --        2048 (-)
PS2636                    1024 (-)      --       1024 (-)     1024 (-)
Pseudomonas aeruginosa
PA01                      1024 (-)      --        512 (-)     1024 (-)
PA124                        --         --       1024 (-)        --

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

Bacterial strains (a)        CHL

Escherichia coli
ATCC8739                   2 (8)#
AG100A                    32 (256)
AG100ATET                 8 (128)#
AGI 02                     32 (-)
W3110                      2 (8)#
MC4100                     2 (8)#
Enterobacter aerogenes
ATCC13048                  2 (8)#
EA289                     128 (128)
EA294                      2 (8)#
EA27                       64 (2)
CM64                       16 (-)
Klebsiella pneumoniae
ATCC11296                  8 (64)#
KP55                       2 (8)#
KP63                       64 (-)
K24                       4 (256)#
Providencia stuartii
PS299645                   32 (-)
NEA16                      32 (-)
PS2636                     32 (-)
Pseudomonas aeruginosa
PA01                      128 (256)
PA124                      32 (-)

(a) Bacterial strain [E.c: Escherichia coli, E.a: Enterobacter
aerogenes, K.p: Klebsiella pneumoniae, Es: Providencia stuartii,
and P.a: Pseudomonas aeruginosa]. (b) Samples [AAS: Aframomum
alboviolaceum (stem), AAL: Aframomum alboviolaceum (leaves),
ALL: Aframomum letestuanum (leaves), CPP: Cucurbitapepo
(pericarps), PPS: Physalisperuviana (stem), RHP: Raphia
hookeri (pericarps), and THL: Tristemma hirtum (leaves);
CHL: chloramphenicol]; MIC: minimal inhibitory concentration;
MBC: minimal bactericidal concentration; -: MIC and MBC > 2048
[micro]g/mL; MIC in #: significant activity.

Table 4: Preliminary evaluation of antibiotic-resistance
modulatory activity of selected extracts at subinhibitory
concentrations against Pseudomonas aeruginosa PA124.

                            MIC of antibiotic ([micro]g/mL) alone
                             and in combination with extracts (a)
                                and fold increase of activity
                                          (in brackets)
Plant        Extract
extracts   concentration     CHL       KAN        CEF        CIP

                 0           128       128        128        64

               MIC/2       32 (4)#   64 (2)#    128 (1)    64 (1)
AAL            MIC/4       64 (2)#   64 (2)#    128 (1)    64 (1)
               MIC/8       64 (2)#   128 (1)    128 (1)    64 (1)
              MIC/16       128 (1)   128 (1)    128 (1)    64 (1)

               MIC/2       128 (1)   64 (2)#    128 (1)    64 (1)
ALL            MIC/4       128 (1)   64 (2)#    128 (1)    64 (1)
               MIC/8       128 (1)   128 (1)    128 (1)    64 (1)
              MIC/16       128 (1)   128 (1)    128 (1)    64 (1)

               MIC/2       32 (4)#   32 (4)#    64 (2)#    32 (2)#
RHP            MIC/4       64 (2)    64 (2)#    128 (1)    64 (1)
               MIC/8       128 (1)   64 (2)#   256 (0.5)   64 (1)
              MIC/16       128 (1)   64 (2)#   256 (0.5)   64 (1)

               MIC/2       8 (16)#   64 (2)#    128 (1)    32 (2)#
THL            MIC/4       8 (16)#   64 (2)#   256 (0.5)   32 (2)#
               MIC/8       32 (4)#   64 (2)#   256 (0.5)   32 (2)#
              MIC/16       32 (4)#   64 (2)#   256 (0.5)   32 (2)#

                            MIC of antibiotic
                          ([micro]g/mL) alone
                           and in combination
                            with extracts (a)
                            and fold increase
                              of activity
                             (in brackets)
Plant        Extract
extracts   concentration    TET        ERY

                 0           16        128

               MIC/2       8 (2)#    128 (1)
AAL            MIC/4       8 (2)#   256 (0.5)
               MIC/8       16 (1)   256 (0.5)
              MIC/16       16(1)    256 (0.5)

               MIC/2       8 (2)#   256 (0.5)
ALL            MIC/4       8 (2)#   256 (0.5)
               MIC/8       16 (1)   256 (0.5)
              MIC/16       16 (1)   256 (0.5)

               MIC/2       8 (2)#    64 (2)#
RHP            MIC/4       16 (1)    128 (1)
               MIC/8       16 (1)    128 (1)
              MIC/16       16 (1)    128 (1)

               MIC/2       8 (2)#    128 (1)
THL            MIC/4       8 (2)#   256 (0.5)
               MIC/8       8 (2)#   256 (0.5)
              MIC/16       8 (2)#   256 (0.5)

(a) Samples [AAL: Aframomum alboviolaceum (leaves), ALL:
Aframomum letestuanum (leaves), RHP: Raphia hookeri (pericarps),
THL: Tristemma hirtum (leaves), CHL: chloramphenicol, CEF:
ceftriaxone, CIP: ciprofloxacin, ERY: erythromycin, KAN:
kanamycin, STR: streptomycin, and TET: tetracycline]; in
brackets: 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 Aframomum alboviolaceum.

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

                                Escherichia coli    Enterobacter
                 Extract                              aerogenes
Antibiotics    concentration    AG100A     AG102        EA289

                     0           256        256          128
CHL               CM 1/2       128 (2)#   64 (4)#      128 (1)
                   CMI/4       128 (2)#   128 (2)#    256 (0.5)

                     0            8          64           64
KAN                CMI/2        8 (1)     32 (2)#     256 (0.25)
                   CMI/4        8 (1)     32 (2)#     256 (0.25)

                     0            64         64           64
CEF                CMI/2      128 (0.5)   4 (16)#     128 (0.5)
                   CMI/4      128 (.05)    8 (8)#     128 (0.5)

                     0            16         16           8
CIP                CMI/2       32 (0.5)    16 (1)      16 (0.5)
                   CMI/4      64 (0.25)    16 (1)      16 (0.5)

                     0           >64         64           32
TET                CMI/2       >64 (1)     64 (1)       32 (1)
                   CMI/4       >64 (1)     64 (1)       32 (1)

                     0           >256       128          >256
ERY                CMI/2       >256 (1)   64 (2)#      >256 (1)
                   CMI/4       >256 (1)   64 (2)#      >256 (1)

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

                               Klebsiella    Providencia
                 Extract       pneumoniae      stuartii
Antibiotics    concentration      KP 63         NEA16

                     0             64            128
CHL               CM 1/2        128 (0.5)      64 (2)#
                   CMI/4        128 (0.5)      128 (1)

                     0             64             64
KAN                CMI/2        128 (0.5)      32 (2)#
                   CMI/4        128 (0.5)      32 (2)#

                     0             128           256
CEF                CMI/2         32 (4)#       64 (4)#
                   CMI/4         64 (2)#       128 (2)#

                     0             32             32
CIP                CMI/2         32 (1)        64 (0.5)
                   CMI/4        64 (0.5)       64 (0.5)

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

                     0             128           128
ERY                CMI/2         128 (1)       16 (8)#
                   CMI/4        256 (0.5)      64 (2)#

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

                                      Pseudomonas aeruginosa
                 Extract
Antibiotics    concentration                   PA01

                     0                         256
CHL               CM 1/2                     32 (8)#
                   CMI/4                     128 (2)#

                     0                          64
KAN                CMI/2                     32 (4)#
                   CMI/4                     32 (4)#

                     0                          64
CEF                CMI/2                     32 (2)#
                   CMI/4                    128 (0.5)

                     0                          16
CIP                CMI/2                     32 (0.5)
                   CMI/4                     32 (0.5)

                     0                         >64
TET                CMI/2        32 ([greater than or equal to] 2)#
                   CMI/4                     >64 (1)

                     0                         >256
ERY                CMI/2        64 ([greater than or equal to] 4)#
                   CMI/4       128 ([greater than or equal to] 2)#

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

                              Pseudomonas
                               aeruginosa
                 Extract                    Modulating
Antibiotics    concentration      PA124      effect (%)

                     0             128
CHL               CM 1/2         32 (4)#       71.42#
                   CMI/4         64 (2)#       42.85

                     0             128
KAN                CMI/2         64 (2)#       57.14
                   CMI/4         64 (2)#       57.14

                     0             128
CEF                CMI/2         128 (1)       57.14
                   CMI/4         128 (1)       42.85

                     0             64
CIP                CMI/2         64 (1)        00.00
                   CMI/4         64 (1)        00.00

                     0             16
TET                CMI/2         8 (2)#        42.85
                   CMI/4         8 (2)#        28.57

                     0             128
ERY                CMI/2         128 (1)       42.85
                   CMI/4        256 (0.5)      42.85

CHL: chloramphenicol, KAN: kanamycin, CEF: ceftriaxone, CIP:
ciprofloxacin, TET: tetracycline, and ERY: erythromycin; in
brackets: 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 Aframomum letestuanum.

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

                                      Escherichia coli
                Extract
Antibiotics   concentration             AG100A               AG102

                    0                    256                  256
CHL               CMI/2                256 (1)              64 (4)#
                  CMI/4                256 (1)              256 (1)

                    0                     8                   64
KAN               CMI/2               32 (0.25)             64 (1)
                  CMI/4               32 (0.25)            128 (0.5)

                    0                     64                  64
CEF               CMI/2       [less than or equal to] 2     16 (4)#
                                  ([greater than or
                                    equal to 32)#
                  CMI/4                 64 (1)              32 (2)#

                    0                     16                  16
CIP               CMI/2                 16 (1)              16 (1)
                  CMI/4                 16 (1)             32 (0.5)

                    0                    >64                  64
TET               CMI/2                >64 (1)             128 (0.5)
                  CMI/4                >64 (1)             128 (0.5)

                    0                    >256                 128
ERY               CMI/2                >256 (1)            128 (0.5)

                  CMI/4                >256 (1)            128 (0.5)

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

                             Enterobacter    Klebsiella   Providencia
                Extract        aerogenes     pneumoniae     stuartii
Antibiotics   concentration      EA289          KP 63         NEA16

                    0             128            64            128
CHL               CMI/2        256 (0.5)     256 (0.25)      128 (1)
                  CMI/4        256 (0.5)     256 (0.25)      128 (1)

                    0              64            64            64
KAN               CMI/2          64 (1)       128 (0.5)     128 (0.5)
                  CMI/4          64 (1)       128 (0.5)     128 (0.5)

                    0              64            128           256
CEF               CMI/2        128 (0.5)       16 (8)#       64 (4)#

                  CMI/4        256 (0.25)      32 (4)#       64 (4)#

                    0              8             32            32
CIP               CMI/2        32 (0.25)      64 (0.5)      64 (0.5)
                  CMI/4        32 (0.25)      64 (0.5)      64 (0.5)

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

                    0             >256           128           128
ERY               CMI/2         >256 (1)       128 (1)       32 (4)#

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

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

                                  Pseudomonas aeruginosa
                Extract
Antibiotics   concentration          PA01            PA124

                    0                256              128
CHL               CMI/2            64 (4)#          128 (1)
                  CMI/4            128 (2)#         128 (1)

                    0                 64              128
KAN               CMI/2            32 (2)#          64 (2)#
                  CMI/4            32 (2)#          64 (2)#

                    0                 64              128
CEF               CMI/2            32 (2)#          128 (1)

                  CMI/4           128 (0.5)         128 (1)

                    0                 16              64
CIP               CMI/2            32 (0.5)         64 (1)
                  CMI/4            32 (0.5)         64 (1)

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

                    0                >256             128
ERY               CMI/2      128 ([greater than    256 (0.5)
                               or equal to] 2)#
                  CMI/4      128 ([greater than    256 (0.5)
                               or equal to] 2)#

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

                Extract       Modulating
Antibiotics   concentration   effect (%)

                    0
CHL               CMI/2          28.57
                  CMI/4          14.28

                    0
KAN               CMI/2          28.57
                  CMI/4          28.57

                    0
CEF               CMI/2         71.42#

                  CMI/4          42.85

                    0
CIP               CMI/2          00.00
                  CMI/4          00.00

                    0
TET               CMI/2          28.57
                  CMI/4          28.57

                    0
ERY               CMI/2          28.57

                  CMI/4          28.57

CHL: chloramphenicol, KAN: kanamycin, CEF: ceftriaxone,
CIP: ciprofloxacin, TET: tetracycline, and ERY: erythromycin;
in brackets: modulating factor; MIC: minimal inhibitory
concentration. Values in # represent modulating factor
[greater than or equal to] 2.

Table 7: Antibiotic-resistance modulatory activity of
pericarps extract of Raphia hookeri.

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

                                Escherichia coli     Enterobacter
                Extract                                aerogenes
Antibiotics   concentration    AG100A       AG102        EA289

                    0            256         256          128
CHL               CMI/2       128 (2)#     32 (8)#      32 (4)#
                  CMI/4       128 (2)#     32 (8)#      32 (4)#

                    0             8          64            64
KAN               CMI/2       32 (0.25)    32 (2)#      32 (2)#
                  CMI/4       32 (0.25)    32 (2)#      32 (2)#

                    0            64          64            64
CEF               CMI/2        64 (1)      4 (32)#       64 (1)
                  CMI/4        64 (1)      4 (32)#       64 (1)

                    0            16          16            8
CIP               CMI/2        8 (2)#     32 (0.5)      16 (0.5)
                  CMI/4        8 (2)#     32 (0.5)      16 (0.5)

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

                  CMI/4        >64 (1)     64 (1)        8 (4)#

                    0           >256         128          >256
ERY               CMI/2       >256 (1)    256 (0.5)     128 (2)#

                  CMI/4       >256 (1)    256 (0.5)     >256 (1)

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

                              Klebsiella   Providencia
                Extract       pneumoniae     stuartii
Antibiotics   concentration      KP63          NEA16

                    0             64            128
CHL               CMI/2         32 (2)#       16 (8)#
                  CMI/4         32 (2)#       16 (8)#

                    0             64            64
KAN               CMI/2         32 (2)#       32 (2)#
                  CMI/4         32 (2)#       32 (2)#

                    0             128           256
CEF               CMI/2         32 (4)#       64 (4)#
                  CMI/4         32 (4)#       64 (4)#

                    0             32            32
CIP               CMI/2         2 (16)#      64 (0.5)
                  CMI/4         2 (16)#      64 (0.5)

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

                  CMI/4         32 (2)#       4 (8)#

                    0             128           128
ERY               CMI/2         64 (2)#       32 (4)#

                  CMI/4         64 (2)#       32 (4)#

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

                                  Pseudomonas aeruginosa
                Extract
Antibiotics   concentration          PA01            PA124

                    0                 256             128
CHL               CMI/2            128 (2)#         32 (4)#
                  CMI/4            128 (2)#         64 (2)#

                    0                 64              128
KAN               CMI/2             128 (1)         32 (4)#
                  CMI/4             128 (1)         64 (2)#

                    0                 64              128
CEF               CMI/2             32 (2)#         64 (2)#
                  CMI/4             32 (2)#         128 (1)

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

                    0                 >64             16
TET               CMI/2       64 ([greater than     8 (2)#
                               or equal to] 2)#
                  CMI/4       64 ([greater than     16 (1)
                               or equal to] 2)#

                    0                >256             128
ERY               CMI/2       128 ([greater than    64 (2)#
                               or equal to] 2)#
                  CMI/4       128 ([greater than    128 (1)
                               or equal to] 2)#

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

                Extract       Modulating
Antibiotics   concentration   effect (%)

                    0
CHL               CMI/2         100.00#
                  CMI/4         100.00#

                    0
KAN               CMI/2         71.42#
                  CMI/4         71.42#

                    0
CEF               CMI/2         71.42#
                  CMI/4          57.14

                    0
CIP               CMI/2          42.85
                  CMI/4          28.57

                    0
TET               CMI/2         71.42#

                  CMI/4          57.14

                    0
ERY               CMI/2         71.42#

                  CMI/4          42.85

CHL: chloramphenicol, KAN: kanamycin, CEF: ceftriaxone, CIP:
ciprofloxacin, TET: tetracycline, and ERY: erythromycin; in
brackets: 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 Tristemma hirtum.

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

                                   Escherichia coli
                Extract
Antibiotics   concentration             AG100A

                    0                    256
CHL               CMI/2                128 (2)#

                  CMI/4                128 (2)#

                    0                     8
KAN               CMI/2       [less than or equal to] 2
                                  ([greater than or
                                    equal to] 4)#
                  CMI/4       [less than or equal to] 2
                                  ([greater than or
                                    equal to] 4)#

                    0                     64
CEF               CMI/2                 8 (8)#

                  CMI/4               128 (0.5)

                    0                     16
CIP               CMI/2                 8 (2)#

                  CMI/4                 8 (2)#

                    0                    >64
TET               CMI/2           32 ([greater than
                                   or equal to] 2)#

                  CMI/4           32 ([greater than
                                   or equal to] 2)#

                    0                    >256
ERY               CMI/2          128 ([greater than
                                   or equal to] 2)#
                  CMI/4          128 ([greater than
                                   or equal to] 2)#

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

                                   Escherichia coli
                Extract
Antibiotics   concentration              AG102

                    0                     256
CHL               CMI/2       [less than or equal to] 2
                                  ([greater than or
                                    equal to] 128)#
                  CMI/4       [less than or equal to] 2
                                  ([greater than or
                                    equal to] 128)#

                    0                     64
KAN               CMI/2                 16 (4)#

                  CMI/4                 16 (4)#

                    0                     64
CEF               CMI/2                 8 (8)#

                  CMI/4                 32 (2)#

                    0                     16
CIP               CMI/2      [less than or equal to] 0.5
                                  ([greater than or
                                    equal to] 32)#
                  CMI/4                 4 (8)#

                    0                     64
TET               CMI/2                 32 (2)#

                  CMI/4                 32 (2)#

                    0                     128
ERY               CMI/2                 8 (16)#

                  CMI/4                 16 (8)#

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

                                     Enterobacter          Klebsiella
                Extract                aerogenes            pneumoniae
Antibiotics   concentration              EA289                 KP63

                    0                     128                   64
CHL               CMI/2                 16 (8)#              16 (4)#

                  CMI/4                 16 (8)#              16 (4)#

                    0                     64                    64
KAN               CMI/2       [less than or equal to] 2      16 (4)#
                                  ([greater than or
                                    equal to] 32)#
                  CMI/4       [less than or equal to] 2      32 (2)#
                                  ([greater than or
                                    equal to] 32)#

                    0                     64                   128
CEF               CMI/2                 8 (8)#               16 (8)#

                  CMI/4                 32 (2)#              32 (4)#

                    0                      8                    32
CIP               CMI/2      [less than or equal to] 0.5      4 (8)#
                                  ([greater than or
                                    equal to] 16)#
                  CMI/4      [less than or equal to] 0.5      4 (8)#
                                  ([greater than or
                                    equal to] 16)#

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

                    0                    >256                  128
ERY               CMI/2           16 ([greater than          32 (4)#
                                   or equal to] 16)#
                  CMI/4           32 ([greater than          32 (4)#
                                   or equal to] 8)#

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

                              Providencia
                Extract         stuartii
Antibiotics   concentration      NEA16

                    0             128
CHL               CMI/2         16 (8)#

                  CMI/4         16 (8)#

                    0              64
KAN               CMI/2         16 (4)#

                  CMI/4         32 (2)#

                    0             256
CEF               CMI/2         32 (8)#

                  CMI/4         32 (8)#

                    0              32
CIP               CMI/2         16 (2)#

                  CMI/4         16 (2)#

                    0              32
TET               CMI/2          4 (8)#

                  CMI/4          4 (8)#

                    0             128
ERY               CMI/2         64 (2)#

                  CMI/4         64 (2)#

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

                                      Pseudomonas aeruginosa
                Extract
Antibiotics   concentration              PAOl                 PA124

                    0                     256                  128
CHL               CMI/2                 64 (4)#              8 (16)#

                  CMI/4                 64 (4)#              8 (16)#

                    0                     64                   128
KAN               CMI/2       [less than or equal to] 2      64 (2)
                                  ([greater than or
                                    equal to] 64)#
                  CMI/4       [less than or equal to] 2      64 (2)
                                  ([greater than or
                                    equal to] 64)#

                    0                     64                   128
CEF               CMI/2       [less than or equal to] 2      128 (1)
                                  ([greater than or
                                    equal to] 32)#
                  CMI/4       [less than or equal to] 2     256 (0.5)
                                  ([greater than or
                                    equal to] 32)#

                    0                     16                   64
CIP               CMI/2      [less than or equal to] 0.5     32 (2)#
                                  ([greater than or
                                    equal to] 32)#
                  CMI/4      [less than or equal to] 0.5     32 (2)#
                                  ([greater than or
                                    equal to] 32)#

                    0                     >64                  16
TET               CMI/2           32 ([greater than          8 (2)#
                                   or equal to] 4)#

                  CMI/4           64 ([greater than          8 (2)#
                                   or equal to] 2)#

                    0                    >256                  128
ERY               CMI/2           32 ([greater than          128 (1)
                                   or equal to] 8)#
                  CMI/4           64 ([greater than         256 (0.5)
                                   or equal to] 4)#

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

                Extract       Modulating
Antibiotics   concentration   effect (%)

                    0
CHL               CMI/2         100.00#

                  CMI/4         100.00#

                    0
KAN               CMI/2         100.00#

                  CMI/4         100.00#

                    0
CEF               CMI/2         85.71#

                  CMI/4         71.42#

                    0
CIP               CMI/2         100.00#

                  CMI/4         100.00#

                    0
TET               CMI/2         100.00#

                  CMI/4         100.00#

                    0
ERY               CMI/2         85.71#

                  CMI/4         85.71#

CHL: chloramphenicol, KAN: kanamycin, CEF: ceftriaxone, CIP:
ciprofloxacin, TET: tetracycline, and ERY: erythromycin; in
brackets: modulating factor; MIC: minimal inhibitory concentration.
Values in # represent modulating factor [greater than or equal to] 2.
COPYRIGHT 2018 Hindawi Limited
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 2018 Gale, Cengage Learning. All rights reserved.

Article Details
Printer friendly Cite/link Email Feedback
Title Annotation:Research Article
Author:Nguenang, Gaelle S.; Mbaveng, Armelle T.; Fankam, Aime G.; Manekeng, Hermione T.; Nayim, Paul; Wamba
Publication:The Scientific World Journal
Date:Jan 1, 2018
Words:7916
Previous Article:A Comparative Analysis of Tooth Size Discrepancy between Male and Female Subjects Presenting with a Class I Malocclusion.
Next Article:Methodology to Evaluate Dripper Sensitivity to Clogging due to Solid Particles: An Assessment.
Topics:

Terms of use | Privacy policy | Copyright © 2020 Farlex, Inc. | Feedback | For webmasters