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2020 Vol.33, Issue 6 Preview Page

Research Article

Assessment of β-Lactamase Inhibitor Potential of Medicinal Plant Extracts against Antibiotic-resistant Staphylococcus aureus
Jirapat Dawan1
,
Juhee Ahn2†
1Graduate Student, Department of Biomedical Science, Kangwon National University, Chuncheon 24341, Korea
2Professor, Department of Biomedical Science and Institute of Bioscience and Biotechnology, Kangwon National University, Chuncheon 24341, Korea
*juheeahn@kangwon.ac.kr
1 December 2020. pp. 578-585
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Abstract

This study was designed to assess the possibility of using medicinal plant extracts as β-lactamase inhibitors to control antibiotic-resistant Staphylococcus aureus. The susceptibilities of S. aureus ATCC 15564 (SAWT), ciprofloxacin-induced S. aureus ATCC 15564 (SACIP), oxacillin-induced S. aureus ATCC 15564 (SAOXA), and clinically-isolated S. aureus CCARM 3008 (SACLI) to ampicillin were determined in the absence and presence of medicinal plant extracts, including Cleyera japonica (CJ), Carpinus laxiflora (CL), Euphorbia helioscopia (EH), Euscaphis japonica (EJ), Oenothera erythrosepala (OE), and Rosa multiflora (RM). The phenotypic change in the clear inhibition zones around ampicillin disc was observed for SAWT, SACIP, and SAOXA, indicating the production of ampicillinase. Compared to the controls, the MICs of ampicillin against SAWT, SACIP, and SAOXA were decreased from 4 to 0.5 ㎍/mL in the presence of CL, 16 to 4 ㎍/mL in the presence of RM, and 32 to 2 ㎍/mL in the presence of CL, EH, and RM, respectively. The medicinal plant extracts, OE, EJ, and CL, effectively inhibited the β-lactamase activities of SAWT (78%), SACIP (57%), and SAOXA (76%) when compared to the control. This results suggest that the medicinal plant extracts can be used as BLIs to control the antibiotic-resistant S. aureus.

Keywords
Ampicillin
Antibiotic resistance
β-Lactamase inhibitor
β-Lactamase activity
Medicinal plant extract
Staphylococcus aureus
References
1
Akova, M. 2008. Sulbactam-containing b-lactamase inhibitor combinations. Clin. Microbiol. Infect. 14:185-88. 10.1111/j.1469-0691.2007.01847.x18154545
2
Amjad, A., I. Mirza, S. Abbasi, U. Farwa, N. Malik and F. Zia. 2011. Modified Hodge test: A simple and effective test for detection of carbapenemase production. Iran J Microbiol 3:189-93.
3
Anderson, K.F., D.R. Lonsway, J.K. Rasheed, J. Biddle, B. Jensen, L.K. McDougal, R.B. Carey, A. Thompson, S. Stocker, B. Limbago and J.B. Patel. 2007. Evaluation of methods to identify the Klebsiella pneumoniae carbapenemase in Enterobacteriaceae. J. Clin. Microbiol. 45:2723-25. 10.1128/JCM.00015-0717581941PMC1951220
4
Aparna, V., K. Dineshkumar, N. Mohanalakshmi, D. Velmurugan and W. Hopper. 2014. Identification of natural compound inhibitors for multidrug efflux pumps of Escherichia coli and Pseudomonas aeruginosa using In silico high-throughput virtual screening and in vitro validation. PLoS One 9:e101840. 10.1371/journal.pone.010184025025665PMC4099075
5
Barry, G.H. and M. Barlow. 2005. Revised Ambler classification of b-lactamases. J. Antimicrob. Chemother. 55:1050-51. 10.1093/jac/dki13015872044
6
Bauernfeind, A. 1986. Classification of β-lactamases. Rev. Infect. Dis. 8:S470-S81. 10.1093/clinids/8.Supplement_5.S470
7
Boussoualim, N. and B. Abderrahmane. 2011. Kinetic study of different flavonoids as inhibitors of beta-lactamase enzyme. Afr. J. Biochem. Res. 5:321-27.
8
Bush, K. and P.A. Bradford. 2016. β-Lactams and β-lactamase inhibitors: An overview. Cold Spring Harbor Perspect. Med. 6:a025247. 10.1101/cshperspect.a02524727329032PMC4968164
9
Catteau, L., N.T. Reichmann, J. Olson, M.G. Pinho, V. Nizet, F. Van Bambeke and J. Quetin-Leclercq. 2017. Synergy between ursolic and oleanolic acids from Vitellaria paradoxa leaf extract and β-lactams against methicillin-resistant Staphylococcus aureus: In vitro and in vivo activity and underlying mechanisms. Molecules 22:2245. 10.3390/molecules2212224529258194PMC6149719
10
Cendrowski, A., K. Kraśniewska, J. Przybył, A. Zielińska and S. Kalisz. 2020. Antibacterial and antioxidant activity of extracts from rose fruits (Rosa rugosa). Molecules 25:E1365. 10.3390/molecules2506136532192161PMC7144371
11
Cheng, M.P., R.S. Lee, A.P. Cheng, S. De L'étoile-Morel, K. Demir, C.P. Yansouni, P. Harris, E.G. McDonald and T.C. Lee. 2019. Beta-lactam/beta-lactamase inhibitor therapy for potential AmpC-producing organisms: A systematic review and meta-analysis. Open Forum Infect. Dis. 6:ofz248. 10.1093/ofid/ofz24831363762PMC6656656
12
CLSI. 2015. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. Approved Standard M07-A10.
13
Elizaquível, P., M. Azizkhani, G. Sánchez and R. Aznar. 2013. Evaluation of Zataria multiflora Boiss. essential oil activity against Escherichia coli O157:H7, Salmonella enterica and Listeria monocytogenes by propidium monoazide quantitative PCR in vegetables. Food Cont. 34:770-776. 10.1016/j.foodcont.2013.06.036
14
Eumkeb, G., S. Sakdarat and S. Siriwong. 2010. Reversing β-lactam antibiotic resistance of Staphylococcus aureus with galangin from Alpinia officinarum Hance and synergism with ceftazidime. Phytomedicine 18:40-45. 10.1016/j.phymed.2010.09.00321036573
15
Eumkeb, G., S. Siriwong, S. Phitaktim, N. Rojtinnakorn and S. Sakdarat. 2012. Synergistic activity and mode of action of flavonoids isolated from smaller galangal and amoxicillin combinations against amoxicillin‐resistant Escherichia coli. J. Appl. Microbiol. 112:55-64. 10.1111/j.1365-2672.2011.05190.x22111967
16
Féria, C., E. Ferreira, J.D. Correia, J. Gonçalves and M. Caniça. 2002. Patterns and mechanisms of resistance to b-lactams and b-lactamase inhibitors in uropathogenic Escherichia coli isolated from dogs in Portugal. J. Antimicrob. Chemother. 49:77-85. 10.1093/jac/49.1.7711751770
17
Fuda, C.C.S., J.F. Fisher and S. Mobashery. 2005. β-Lactam resistance in Staphylococcus aureus: The adaptive resistance of a plastic genome. Cell. Mol. Life Sci. 62:2617. 10.1007/s00018-005-5148-616143832
18
Hanson, N.D. and C.C. Sanders. 1999. Regulation of inducible AmpC beta-lactamase expression among Enterobacteriaceae. Curr. Pharmaceut. Design. 5:881-894.
19
Hou, W.C., R.D. Lin, K.T. Cheng, Y.T. Hung, C.H. Cho, C.H. Chen, S.Y. Hwang and M.H. Lee. 2003. Free radical-scavenging activity of Taiwanese native plants. Phytomedicine 10:170-175. 10.1078/09447110332165989812725572
20
Lamers, R.P., J.F. Cavallari and L.L. Burrows. 2013. The efflux inhibitor phenylalanine-arginine beta-naphthylamide (PAβN) permeabilizes the outer membrane of gram-negative bacteria. PLoS One 8:e60666. 10.1371/journal.pone.006066623544160PMC3609863
21
Lee, S.-H., T.-W. Jang, J.-S. Choi, J.-Y. Mun and J.-H. Park. 2019. Inhibitory effects of pine cone Pinus densiflora on melanogenesis in B16F10 melanoma cells. Korean J. Plant Res. 32:275-81.
22
Liu, X., K. Thungrat and D.M. Boothe. 2016. Occurrence of OXA-48 carbapenemase and other b-lactamase genes in ESBL-producing multidrug resistant Escherichia coli from dogs and cats in the United States, 2009-2013. Front. Microbiol. 7:1057. 10.3389/fmicb.2016.01057
23
Llarrull, L.I., J.F. Fisher and S. Mobashery. 2009. Molecular basis and phenotype of methicillin resistance in Staphylococcus aureus and insights into new β-lactams that meet the challenge. Antimicrob. Agent Chemother. 53:4051-63. 10.1128/AAC.00084-0919470504PMC2764218
24
Manchanda, V. and N.P. Singh. 2003. Occurrence and detection of AmpC b-lactamases among Gram-negative clinical isolates using a modified three-dimensional test at Guru Tegh Bahadur Hospital, Delhi, India. J. Antimicrob. Chemother. 51:415-18. 10.1093/jac/dkg09812562713
25
Matsumoto, Y., K. Hayama, S. Sakakihara, K. Nishino, H. Noji, R. Iino and A. Yamaguchi. 2011. Evaluation of multidrug efflux pump inhibitors by a new method using microfluidic channels. PLoS One 6:e18547. 10.1371/journal.pone.001854721533264PMC3075257
26
Michéa-Hamzehpour, M., A. Kahr and J.C. Pechère. 1994. In vitro stepwise selection of resistance to quinolones, β-lactams and amikacin in nosocomial gram-negative bacilli. Infection 22:S105-S110. 10.1007/BF017935747927828
27
Payne, D.J., R. Cramp, J.H. Bateson, J. Neale and D. Knowles. 1994. Rapid identification of metallo- and serine b-lactamases. Antimicrob. Agent. Chemother. 38:991-96. 10.1128/AAC.38.5.9918067782PMC188139
28
Rubens, D.M., O.O. Constantin, A.-A. Moevi, G.K. Nathalie, T. Daouda, N.J. David, D. Mireille and D.A. Joseph. 2015. Anti Staphylococcus aureus activity of the aqueous extract and hexanic fraction of Thonningia sanguinea (Cote ivoire). Int. J. Pharmaco. Phytochem. Res. 7:301-06.
29
Rumbo, C., E. Gato, M. López, C. Ruiz de Alegría, F. Fernández-Cuenca, L. Martínez-Martínez, J. Vila, J. Pachón, J.M. Cisneros, J. Rodríguez-Baño, A. Pascual, G. Bou and M. Tomás. 2013. Contribution of efflux pumps, porins, and b-lactamases to multidrug resistance in clinical isolates of Acinetobacter baumannii. Antimicrob. Agent. Chemother. 57:5247-5257. 10.1128/AAC.00730-1323939894PMC3811325
30
Sibanda, T. and A. Okoh. 2007. The challenges of overcoming antibiotic resistance: Plant extracts as potential sources of antimicrobial and resistance modifying agents. Afr. J. Biotechnol. 6:2886-2896.
31
Sood, S. 2013. Comparative evaluation of the in-vitro activity of six β-lactam/β-lactamase inhibitor combinations against Gram negative Bacilli. J. Clin. Diagn. Res. 7:224-28. 10.7860/JCDR/2013/4564.273323543071PMC3592279
32
Stapleton, P., S. Shah, J. Anderson, Y. Hara, J. Hamilton-Miller and P. Taylor. 2004. Modulation of b-lactam resistance in Staphylococcus aureus by catechins and gallates. Int. J. Antimicrob. Agents 23:462-67. 10.1016/j.ijantimicag.2003.09.02715120724
33
Sun, S., M. Selmer and D.I. Andersson. 2014. Resistance to β-lactam antibiotics conferred by point mutations in penicillin-binding proteins PBP3, PBP4 and PBP6 in Salmonella enterica. PLoS One 9:e97202. 10.1371/journal.pone.009720224810745PMC4014608
34
Venkatesan, A.M., A. Agarwal, T. Abe, H. Ushirogochi, I. Yamamura, T. Kumagai, P.J. Petersen, W.J. Weiss, E. Lenoy, Y. Yang, D.M. Shlaes, J.L. Ryan and T.S. Mansour. 2004. Novel imidazole substituted 6-methylidene-penems as broad-spectrum β-lactamase inhibitors. Bioorg. Med. Chem. 12:5807-5817. 10.1016/j.bmc.2004.08.03915498657
35
Zabawa, T.P., M.J. Pucci, T.R. Parr and T. Lister. 2016. Treatment of Gram-negative bacterial infections by potentiation of antibiotics. Curr. Opin. Microbiol. 33:7-12. 10.1016/j.mib.2016.05.00527232956
36
Zhao, W.-H., Z.-Q. Hu, Y. Hara and T. Shimamura. 2002. Inhibition of penicillinase by epigallocatechin gallate resulting in restoration of antibacterial activity of penicillin against penicillinase-producing Staphylococcus aureus. Antimicrob. Agent Chemother. 46:2266-68. 10.1128/AAC.46.7.2266-2268.200212069986PMC127279
Information
  • Publisher :The Plant Resources Society of Korea
  • Publisher(Ko) :한국자원식물학회
  • Journal Title :Korean Journal of Plant Resources
  • Journal Title(Ko) :한국자원식물학회지
  • Volume : 33
  • No :6
  • Pages :578-585
  • Received Date : 2020-05-20
  • Revised Date : 2020-09-14
  • Accepted Date : 2020-09-14
  • DOI :https://doi.org/10.7732/kjpr.2020.33.6.578
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