Antibacterial and Synergy of Berberines with Antibacterial Agents against Clinical Multi-Drug Resistant Isolates of Methicillin-Resistant Staphylococcus aureus (MRSA)
Abstract
:1. Introduction
2. Results and Discussion
Strain NO. | MRSA 004 | MRSA 055 | MRSA 123 | MRSA 144 | MRSA 189 | MRSA 240 | MRSA 276 | MRSA 294 | MRSA 328 | MRSA 330 | MRSAs (50%) | MRSAs (90%) | ATCC 25923 | |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Ber b | MIC | 64 | 128 | 32 | 128 | 64 | 64 | 32 | 32 | 32 | 64 | 64 | 128 | 64 |
MBC | 128 | 256 | 256 | 256 | 128 | 64 | 128 | 64 | 256 | 256 | 128 | 256 | 128 | |
A-Ber | MIC | 64 | 32 | 64 | 64 | 64 | 128 | 32 | 32 | 32 | 32 | 32 | 64 | 64 |
MBC | 512 | 256 | 256 | 512 | 128 | 128 | 128 | 128 | 256 | 256 | 256 | 512 | 512 | |
AMP | MIC | 64 | 128 | 64 | 64 | 64 | 64 | 64 | 128 | 128 | 64 | 64 | 128 | 16 |
MBC | 512 | 512 | 256 | 256 | 512 | 512 | 512 | 512 | 512 | 512 | 512 | 512 | 64 | |
CFZ | MIC | 128 | 128 | 128 | 256 | 256 | 128 | 256 | 128 | 128 | 256 | 128 | 256 | 128 |
MBC | nt | nt | nt | nt | nt | nt | nt | nt | nt | nt | nt | nt | nt | |
LEV | MIC | 8 | 16 | 32 | 16 | 32 | 16 | 16 | 16 | 16 | 8 | 16 | 32 | 2 |
MBC | 64 | 64 | 64 | 64 | 64 | 64 | 64 | 64 | 64 | 64 | 64 | 64 | 8 | |
AZM | MIC | 4,000 | 4,000 | 2,000 | 4,000 | 4,000 | 4,000 | 4,000 | 4,000 | 2,000 | 4,000 | 4,000 | 4,000 | 4,000 |
MBC | Nt c | nt | nt | nt | nt | nt | nt | nt | nt | nt | nt | nt | nt | |
VAN | MIC | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 |
MBC | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 |
Strain NO. | MRSA | MRSA | MRSA | MRSA | MRSA | MRSA | MRSA | MRSA | MRSA | MRSA | MRSAs | MRSAs |
---|---|---|---|---|---|---|---|---|---|---|---|---|
004 | 055 | 123 | 144 | 189 | 240 | 276 | 294 | 328 | 330 | (50%) | (90%) | |
Ber a | 16 | 16 | 4 | 32 | 16 | 16 | 8 | 8 | 8 | 16 | 16 | 16 |
LEV | 2 | 4 | 8 | 4 | 8 | 8 | 4 | 2 | 2 | 2 | 4 | 8 |
Effect | syn | syn | syn | syn | syn | add | syn | syn | syn | syn | syn | syn |
FICI b | 0.500 | 0.375 | 0.375 | 0.500 | 0.500 | 0.750 | 0.500 | 0.375 | 0.375 | 0.500 | 0.500 | 0.500 |
Rd% (Ber) c | 75.0 | 87.5 | 87.5 | 75.0 | 75.0 | 75.0 | 75.0 | 75.0 | 75.0 | 75.0 | >75.0 | >75.0 |
Rd% (LEV) | 75.0 | 75.0 | 75.0 | 75.0 | 75.0 | 50.0 | 75.0 | 87.5 | 87.5 | 75.0 | >75.0 | >75.0 |
Ber | 16 | 16 | 4 | 16 | 8 | 32 | 8 | 8 | 4 | 8 | 8 | 16 |
AZM | 500 | 500 | 250 | 1000 | 1000 | 500 | 500 | 1000 | 250 | 250 | 500 | 1000 |
FICI | 0.375 | 0.250 | 0.250 | 0.375 | 0.375 | 0.625 | 0.375 | 0.500 | 0.250 | 0.188 | 0.375 | 0.500 |
Effect | syn | syn | syn | syn | syn | add | syn | syn | syn | syn | syn | syn |
Rd% (Ber) | 75.0 | 87.5 | 87.5 | 87.5 | 87.5 | 50.0 | 75.0 | 75.0 | 87.5 | 87.5 | 87.5 | >75.0 |
Rd% (AZM) | 87.5 | 87.5 | 87.5 | 75.0 | 75.0 | 87.5 | 87.5 | 75.0 | 87.5 | 93.8 | >87.5 | >75.0 |
A-Ber | 8 | 4 | 4 | 16 | 8 | 32 | 8 | 8 | 4 | 8 | 8 | 16 |
LEV | 2 | 2 | 4 | 4 | 2 | 4 | 4 | 4 | 4 | 2 | 4 | 4 |
FICI | 0.375 | 0.250 | 0.188 | 0.500 | 0.188 | 0.500 | 0.500 | 0.500 | 0.375 | 0.500 | 0.375 | 0.500 |
Effect | syn | syn | syn | syn | syn | syn | syn | syn | syn | syn | syn | syn |
Rd% (A-Ber) | 87.5 | 87.5 | 93.8 | 75.0 | 87.5 | 75.0 | 75.0 | 75.0 | 87.5 | 75.0 | >87.5 | >75.0 |
Rd% (LEV) | 75.0 | 87.5 | 87.5 | 75.0 | 93.8 | 75.0 | 75.0 | 75.0 | 75.0 | 75.0 | >75.0 | >75.0 |
A-Ber | 16 | 4 | 16 | 8 | 16 | 32 | 8 | 8 | 8 | 8 | 8 | 16 |
AZM | 125 | 125 | 250 | 1000 | 1000 | 1000 | 500 | 125 | 500 | 250 | 250 | 1000 |
FICI | 0.281 | 0.156 | 0.375 | 0.375 | 0.500 | 0.500 | 0.375 | 0.281 | 0.500 | 0.313 | 0.375 | 0.500 |
Effect | syn | syn | syn | syn | syn | syn | syn | syn | syn | syn | syn | syn |
Rd% (A-Ber) | 75.0 | 87.5 | 75.0 | 87.5 | 75.0 | 75.0 | 75.0 | 75.0 | 75.0 | 75.0 | >75.0 | >75.0 |
Rd% (AZM) | 96.9 | 96.9 | 87.5 | 75.0 | 75.0 | 75.0 | 87.5 | 96.9 | 75.0 | 93.8 | >87.5 | >75.0 |
3. Experimental
3.1. Antibacterial Agents
3.2. Bacterial Strains
3.3. Media
3.4. Susceptibility Testing
3.5. Synergy Testing
4. Conclusions
Acknowledgments
Conflict of Interest
References
- Jevons, M.P. “Celbenin”-resistant staphylococci. Br. Med. J. 1961, 124, 124–125. [Google Scholar] [CrossRef]
- Chang, S.; Sievert, D.M.; Hageman, J.C.; Boulton, M.L.; Tenover, F.C.; Downes, F.P.; Shah, S.; Rudrik, J.T.; Pupp, G.R.; Brown, W.J.; et al. Infection with vancomycin-resistant Staphylococcus aureus containing the vanA resistance gene. N. Engl. J. Med. 2003, 348, 1342–1347. [Google Scholar]
- Mahady, G.B. Medicinal plants for the prevention and treatment of bacterial infections. Curr. Pharm. Des. 2005, 11, 2405–2427. [Google Scholar] [CrossRef]
- Gibbons, S. Anti-Staphylococcal plant natural products. Nat. Prod. Rep. 2004, 21, 263–277. [Google Scholar] [CrossRef]
- Gibbons, S. Phytochemicals for bacterial resistance-strengths, weaknesses and opportunities. Planta Med. 2008, 74, 594–602. [Google Scholar] [CrossRef]
- Zuo, G.-Y.; Meng, F.-Y.; Hao, X.-Y.; Zhang, Y.-L.; Wang, G.-C.; Xu, G.-L. Antibacterial alkaloids from Chelidonium majus Linn (Papaveraceae) against clinical isolates of methicillin-resistant Staphylococcus aureus. J. Pharm. Pharm. Sci. 2008, 11, 90–94. [Google Scholar]
- Zuo, G.-Y.; Wang, G.-C.; Zhao, Y.-B.; Xu, G.-L.; Hao, X.-Y.; Han, J.; Zhao, Q. Screening of Chinese medicinal plants for inhibition against clinical isolates of methicillin-resistant Staphylococcus aureus (MRSA). J. Ethnopharmacol. 2008, 120, 287–290. [Google Scholar] [CrossRef]
- Zuo, G.-Y.; Zhang, X.-J.; Yang, C.-X.; Han, J.; Wang, G.-C.; Bian, Z.-Q. Evaluation of traditional Chinese medicinal plants for anti-MRSA activity with reference to the treatment record of infectious diseases. Molecules 2012, 17, 2955–2967. [Google Scholar]
- Zuo, G.-Y.; Li, Y.; Wang, T.; Han, J.; Wang, G.-C.; Zhang, Y.-L.; Pan, W.-D. Synergistic antibacterial and antibacterial agent effects of bisbenzylisoquinoline alkaloids on clinical isolates of methicillin-resistant Staphylococcus aureus (MRSA). Molecules 2011, 16, 9819–9826. [Google Scholar]
- An, J.; Zuo, G.-Y.; Hao, X.-Y.; Wang, G.-C.; Li, Z.-S. Antibacterial and synergy of a flavanonol rhamnoside with antibacterial agents against clinical isolates of methicillin-resistant Staphylococcus aureus (MRSA). Phytomedicine 2011, 18, 990–993. [Google Scholar]
- Yu, H.H.; Kim, K.J.; Cha, J.D.; Kim, H.K.; Lee, Y.E.; Choi, N.Y.; You, Y.O. Antimicrobial activity of berberine alone and in combination with ampicillin or oxacillin against methicillin-resistant Staphylococcus aureus. J. Med. Food 2005, 8, 454–461. [Google Scholar]
- Inoue, K.; Kulsum, U.; Chowdhury, S.A.; Fujisawa, S.-I.; Ishihara, M.; Yokoe, I.; Sakagam, H. Tumor-specific cytotoxicity and apoptosis-inducing activity of berberines. Anticancer Res. 2005, 25, 4053–4060. [Google Scholar]
- McDonald, M.; Dougall, A.; Holt, D.; Huygens, F.; Oppedisano, F.; Giffard, P.M.; Inman-Bamber, J.; Stephens, A.J.; Towers, R.; Carapetis, J.R. Use of single nucleotide polymorphism (SNP) genotyping system to demonstrate the unique epidemiology of methicillin-resistant Staphylococcus aureus in remote Aboriginal communities. J. Clin. Microbiol. 2006, 44, 3720–3727. [Google Scholar] [CrossRef]
- Petersen, P.J.; Labthavikul, P.; Jones, C.H.; Bradford, P.A. In vitro antibacterial activities of tigecycline in combination with other antimicrobial agents determined by chequerboard and time-kill kinetic analysis. J. Antimicrob. Chemother. 2006, 57, 573–576. [Google Scholar]
- Wagner, H.; Ulrich-Merzenich, G. Synergy research: approaching a new generation of phytopharmaceuticals. Phytomedicine 2009, 16, 97–110. [Google Scholar]
- Stavri, M.; Piddock, L.J.V.; Gibbons, S. Bacterial efflux pump inhibitors from natural sources. J. Antimicrob. Chemother. 2007, 59, 1247–1260. [Google Scholar]
- Hemaiswarya, S.; Kruthiventi, A.K.; Doble, M. Synergism between natural products and antibacterial agents against infectious diseases. Phytomedicine 2008, 15, 639–652. [Google Scholar] [CrossRef]
- Onda, M.; Yuasa, K.; Okada, J.; Kataoka, K.; Abe, K. Utilization of protopine and related alkaloids. VI. Chem. Pharm. Bull. 1973, 21, 1333–1337. [Google Scholar]
- Kloos, W.K.; Bannerman, T.L. Staphylococcus and Micrococcus. In Manual of Clinical Microbiology, 7th; Murray, P.R., Baron, E.J., Pfaller, M.A., Tenover, F.C., Yolken, R.H., Eds.; ASM Press: Washington, DC, USA, 1999; pp. 264–282. [Google Scholar]
- Performance Standards for Antimicrobial Disk Susceptibility Tests, Approved standard; CLSI: Wayne, PA, USA, 2006.
- Performance Standards for Antimicrobial Susceptibility Tests, 17th informational supplement; CLSI: Wayne, PA, USA, 2007.
- Zhang, K.; McClure, J.A.; Elsayed, S.; Louie, T.; Conly, J.M. Novel multiplex PCR assay for characterization and concomitant subtyping of staphylococcal cassette chromosome mec types I to V in methicillin-resistant Staphylococcus aureus. J. Clin. Microbiol. 2005, 43, 5026–5033. [Google Scholar]
- Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically, 7th ed; CLSI: Wayne, PA, USA, 2006.
- Methods for Determining Bactericidal Activity of Antimicrobial Agents, Approved Guideline; CLSI: Wayne, PA, USA, 1999.
- Hu, Z.Q.; Zhao, W.H.; Asano, N.; Yoda, Y.; Hara, Y.; Shimamura, T. Epigallocatechin gallate synergistically enhances the activity of carbapenems against methicillin resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 2002, 46, 558–560. [Google Scholar]
- Chin, J.N.; Jones, R.N.; Sader, H.S.; Savage, P.B.; Rybak, M.J. Potential synergy activity of the novel ceragenin, CAS-13, against clinical isolates of Pseudomonas aeruginosa, including multidrug-resistant P. aeruginosa. J. Antimicrob. Chemother. 2008, 61, 365–370. [Google Scholar]
- Sample Availability: Samples of the Ber A-Ber are available from the authors.
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Zuo, G.-Y.; Li, Y.; Han, J.; Wang, G.-C.; Zhang, Y.-L.; Bian, Z.-Q. Antibacterial and Synergy of Berberines with Antibacterial Agents against Clinical Multi-Drug Resistant Isolates of Methicillin-Resistant Staphylococcus aureus (MRSA). Molecules 2012, 17, 10322-10330. https://doi.org/10.3390/molecules170910322
Zuo G-Y, Li Y, Han J, Wang G-C, Zhang Y-L, Bian Z-Q. Antibacterial and Synergy of Berberines with Antibacterial Agents against Clinical Multi-Drug Resistant Isolates of Methicillin-Resistant Staphylococcus aureus (MRSA). Molecules. 2012; 17(9):10322-10330. https://doi.org/10.3390/molecules170910322
Chicago/Turabian StyleZuo, Guo-Ying, Yang Li, Jun Han, Gen-Chun Wang, Yun-Ling Zhang, and Zhong-Qi Bian. 2012. "Antibacterial and Synergy of Berberines with Antibacterial Agents against Clinical Multi-Drug Resistant Isolates of Methicillin-Resistant Staphylococcus aureus (MRSA)" Molecules 17, no. 9: 10322-10330. https://doi.org/10.3390/molecules170910322