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Research Article

PLGA microsphere-based composite hydrogel for dual delivery of ciprofloxacin and ginsenoside Rh2 to treat Staphylococcus aureus-induced skin infections

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Pages 632-641 | Received 15 Mar 2020, Accepted 14 Apr 2020, Published online: 24 Apr 2020

References

  • Årdal C, Balasegaram M, Laxminarayan R, et al. (2019). Antibiotic development—economic, regulatory and societal challenges. Nat Rev Microbiol.18:267–74.
  • Astolfi A, Felicetti T, Iraci N, et al. (2017). Pharmacophore-based repositioning of approved drugs as novel Staphylococcus aureus NorA efflux pump inhibitors. J Med Chem 60:1598–604.
  • Cao XX, Ye QL, Fan MW, et al. (2019). Antimicrobial effects of the ginsenoside Rh2 on monospecies and multispecies cariogenic biofilms. J Appl Microbiol 126:740–51.
  • Cebrián L, Rodríguez JC, Escribano I, et al. (2005). Characterization of Salmonella spp. Mutants with reduced fluoroquinolone susceptibility: importance of efflux pump mechanisms. Chemotherapy 51:40–3.
  • Deepika MS, Thangam R, Sakthidhasan P, et al. (2018). Combined effect of a natural flavonoid rutin from Citrus sinensis and conventional antibiotic gentamicin on Pseudomonas aeruginosa biofilm formation. Food Control 90:282–94.
  • Du DJ, Wang-Kan X, Neuberger A, et al. (2018). Multidrug efflux pumps: structure, function and regulation. Nat Rev Microbiol 16:523–39.
  • Felicetti T, Cannalire R, Burali MS, et al. (2017). Searching for novel inhibitors of the S. aureus NorA efflux pump: synthesis and biological evaluation of the 3-phenyl-1,4-benzothiazine analogues. ChemMedChem 12:1293–302.
  • Felicetti T, Cannalire R, Pietrella D, et al. (2018). 2-Phenylquinoline S. aureus NorA efflux pump inhibitors: evaluation of the importance of methoxy group introduction. J Med Chem 61:7827–48.
  • Fernández L, Hancock RE. (2012). Adaptive and mutational resistance: role of porins and efflux pumps in drug resistance. Clin Microbiol Rev 25:661–81.
  • Foster TJ. (2017). Antibiotic resistance in Staphylococcus aureus. Current status and future prospects. FEMS Microbiol Rev 41:430–49.
  • Gao G, Jiang YW, Jia HR, et al. (2019). Near-infrared light-controllable on-demand antibiotics release using thermo-sensitive hydrogel-based drug reservoir for combating bacterial infection. Biomaterials 188:83–95.
  • Gold K, Slay B, Knackstedt M, et al. (2018). Antimicrobial activity of metal and metal-oxide based nanoparticles. Adv Therap 1:1700033.
  • Holler JG, Christensen SB, Slotved HC, et al. (2012). Novel inhibitory activity of the Staphylococcus aureus NorA efflux pump by a kaempferol rhamnoside isolated from Persea lingue Nees. J Antimicrob Chemoth 67:1138–44.
  • Kim JH, Yi YS, Kim MY, et al. (2017). Role of ginsenosides, the main active components of Panax ginseng, in inflammatory responses and diseases. J Ginseng Res 41:435–43.
  • Kumar S, Lekshmi M, Parvathi A, et al. (2020). Functional and structural roles of the major facilitator superfamily bacterial multidrug efflux pumps. Microorganisms 8:266.
  • LaBreck PT, Bochi-Layec AC, Stanbro J, et al. (2020). Systematic analysis of efflux pump-mediated antiseptic resistance in Staphylococcus aureus suggests a need for greater antiseptic stewardship. mSphere 5:e00959–e00919.
  • Lakhundi S, Zhang KY. (2018). Methicillin-resistant Staphylococcus aureus: molecular characterization, evolution, and epidemiology. Clin Microbiol Rev 31:e00018–00020.
  • Langeveld WT, Veldhuizen EJ, Burt SA. (2014). Synergy between essential oil components and antibiotics: a review. Crit Rev Microbiol 40:76–94.
  • Lee H, Lee S, Jeong D, et al. (2018). Ginsenoside Rh2 epigenetically regulates cell-mediated immune pathway to inhibit proliferation of MCF-7 breast cancer cells. J Ginseng Res 42:455–62.
  • Li YH, Su TT, Zhang Y, et al. (2015). Liposomal co-delivery of daptomycin and clarithromycin at an optimized ratio for treatment of methicillin-resistant Staphylococcus aureus infection. Drug Deliv 22:5.
  • Liu YF, Wang LJ, Liu JP, et al. (2013). A study of human skin and surface temperatures in stable and unstable thermal environments. J Therm Biol 38:440–8.
  • Lu C, Quan GL, Su M, et al. (2019). Molecular architecture and charging effects enhance the in vitro and in vivo performance of multi-arm antimicrobial agents based on star-shaped poly(L-Lysine). Adv Therap 2:1900147.
  • Matthew JE, Nazario YL, Roberts SC, et al. (2002). Effect of mammalian cell culture medium on the gelation properties of Pluronic® F127. Biomaterials 23:4615–9.
  • Mei LL, Chen JT, Yu SQ, et al. (2017). Expansible thermal gelling foam aerosol for vaginal drug delivery. Drug Deliv 24:1325–37.
  • Mir M, Ahmed N, Permana AD, et al. (2019). Enhancement in site-specific delivery of carvacrol against methicillin resistant Staphylococcus aureus induced skin infections using enzyme responsive nanoparticles: a proof of concept study. Pharmaceutics 11:606.
  • Mona GA, Hadeel AM, Nagia NA. (2020). Preparation of PLGA-chitosan based nanocarriers for enhancing antibacterial effect of ciprofloxacin in root canal infection. Drug Deliv 27:26–39.
  • Ng VW, Ke XY, Lee AL, et al. (2013). Synergistic co-delivery of membrane-disrupting polymers with commercial antibiotics against highly opportunistic bacteria. Adv Mater 25:6730–6.
  • Palazzotti D, Bissaro M, Bolcato G, et al. (2019). Deciphering the molecular recognition mechanism of multidrug resistance Staphylococcus aureus NorA efflux pump using a supervised molecular dynamics approach. IJMS 20:4041.
  • Pei YH, Mohamed MF, Seleem MN, et al. (2017). Particle engineering for intracellular delivery of vancomycin to methicillin-resistant Staphylococcus aureus (MRSA)-infected macrophages. J Control Release 267:133–43.
  • Redgrave LS, Sutton SB, Webber MA, et al. (2014). Fluoroquinolone resistance: mechanisms, impact on bacteria, and role in evolutionary success. Trends Microbiol 22:438–45.
  • Rowe SE, Wagner NJ, Li LP, et al. (2020). Reactive oxygen species induce antibiotic tolerance during systemic Staphylococcus aureus infection. Nat Microbiol 5:282–9.
  • Russo A, Concia E, Cristini F, et al. (2016). Current and future trends in antibiotic therapy of acute bacterial skin and skin-structure infections. Clin Microbiol Infect 22:S27–S36.
  • Schindler BD, Jacinto PL, Buensalido JA, et al. (2015). Clonal relatedness is a predictor of spontaneous multidrug efflux pump gene overexpression in Staphylococcus aureus. Int J Antimicrob Agents 45:464–70.
  • Sharma M, Sahu K, Singh SP, et al. (2018). Wound healing activity of curcumin conjugated to hyaluronic acid: in vitro and in vivo evaluation. Artif Cells Nanomed Biotechnol 46:1009–17.
  • Shriram V, Khare T, Bhagwat R, et al. (2018). Inhibiting bacterial drug efflux pumps via phyto-therapeutics to combat threatening antimicrobial resistance. Front Microbiol 9:2990
  • Singer AJ, Talan DA. (2014). Management of skin abscesses in the era of methicillin-resistant Staphylococcus aureus. N Engl J Med 370:1039–47.
  • Singh S, Kalia NP, Joshi P, et al. (2017). Boeravinone B, a novel dual inhibitor of NorA bacterial efflux pump of Staphylococcus aureus and human P-glycoprotein, reduces the biofilm formation and intracellular invasion of bacteria. Front Microbiol 8:1868
  • Tong SY, Davis JS, Eichenberger E, et al. (2015). Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management. Clin Microbiol Rev 28:603–61.
  • Willers C, Wentzel JF, Du Plessis LH, et al. (2017). Efflux as a mechanism of antimicrobial drug resistance in clinical relevant microorganisms: the role of efflux inhibitors. Expert Opin Ther Targets 21:23–36.
  • Wright GD. (2017). Opportunities for natural products in 21st century antibiotic discovery. Nat Prod Rep 34:694–701.
  • Xu HJ, Huang SH, Wang JJ, et al. (2019). Enhanced cutaneous wound healing by functional injectable thermo-sensitive chitosan-based hydrogel encapsulated human umbilical cord-mesenchymal stem cells. Int J Biol Macromol 137:433–41.
  • Xue P, Yang XS, Zhao L, et al. (2020). Relationship between antimicrobial activity and amphipathic structure of ginsenosides. Ind Crops Prod 143:111929.
  • Zeng YM, Chen JT, Li YR, et al. (2018). Thermo-sensitive gel in glaucoma therapy for enhanced bioavailability: in vitro characterization, in vivo pharmacokinetics and pharmacodynamics study. Life Sci 212:80–6.
  • Zhang JW, Sun Y, Wang YY, et al. (2014). Non-antibiotic agent ginsenoside 20(S)-Rh2 enhanced the antibacterial effects of ciprofloxacin in vitro and in vivo as a potential NorA inhibitor. Eur J Pharmacol 740:277–84.
  • Zhu CE, Huang Y, Zhang XY, et al. (2015). Comparative studies on exenatide-loaded poly (D,L-lactic-co-glycolic acid) microparticles prepared by a novel ultra-fine particle processing system and spray drying. Colloids Surf B 132:103–10.