Effects of subinhibitory concentrations of ceftaroline on Methicillin-Resistant Staphylococcus aureus (MRSA) biofilms

PLoS ONE

Volumn 11, Issue 1, 2016, Pages

  Lazaro Diez, Maria ^a   Remuzgo Martinez, Sara ^a   Rodriguez Mirones, Cristina ^a,b   Acosta, Felix ^c   Icardo, Jose M ^d   Martinez Martinez, Luis ^a,b,d   Ramos Vivas, Jose ^a,b  

^a HOSPITAL UNIVERSITARIO MARQUÉS DE VALDECILLA   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c UNIVERSITY OF LAS PALMAS DE GRAN CANARIA   (Spain)

^d UNIVERSITY OF CANTABRIA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CEFTAROLINE; ANTIINFECTIVE AGENT; CEPHALOSPORIN DERIVATIVE;

AGRA GENE; ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BIOFILM; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CORRELATIONAL STUDY; GENE EXPRESSION; ICAA GENE; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; SARA GENE; SASF GENE; SCANNING ELECTRON MICROSCOPY; STRUCTURE ANALYSIS; TRANSMISSION ELECTRON MICROSCOPY; DRUG EFFECTS; MICROBIAL SENSITIVITY TEST;

ANTI-BACTERIAL AGENTS; BIOFILMS; CEPHALOSPORINS; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIAL SENSITIVITY TESTS;

EID: 84958231161     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0147569     Document Type: Article

References (44)

1. Stefani S, Varaldo PE. Epidemiology of methicillin-resistant staphylococci in Europe. Clin Microbiol Infect. 2003; 9:1179-1186. PMID: 14686982.
2. Archer NK, Mazaitis MJ, Costerton JW, Leid JG, Powers ME, Shirtliff ME. Staphylococcus aureus bio-films: properties, regulation, and roles in human disease. Virulence. 2011; 2: 445-459. PMID: 21921685. doi: 10.4161/viru.2.5.17724
3. Lewis K. Multidrug tolerance of biofilms and persister cells. Curr Top Microbiol Immunol. 2008; 322: 107-131. PMID: 18453274.
4. Van Acker H, Van Dijck P, Coenye T. Molecular mechanisms of antimicrobial tolerance and resistance in bacterial and fungal biofilms. Trends Microbiol. 2014; 22: 326-333. PMID: 24598086. doi: 10.1016/j. tim.2014.02.001
5. Hoiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O. Antibiotic resistance of bacterial biofilms. Int J Anti-microb Agents. 2010; 35: 322-332. PMID: 20149602. doi: 10.1016/j.ijantimicag.2009.12.011
6. O'Neill E, Pozzi C, Houston P, Smyth D, Humphreys H, Robinson DA, et al. Association between methi-cillin susceptibility and biofilm regulation in Staphylococcus aureus isolates from device-related infections. J Clin Microbiol. 2007; 45: 1379-1388. PMID: 17329452.
7. O'Gara JP. ica and beyond: biofilm mechanisms and regulation in Staphylococcus epidermidis and Staphylococcus aureus. FEMS Microbiol Lett. 2007; 270:179-188. PMID: 17419768.
8. Valle J, Latasa C, Gil C, Toledo-Arana A, Solano C, Penades JR, et al. Bap, a biofilm matrix protein of Staphylococcus aureus prevents cellular internalization through binding to GP96 host receptor. PloS Pathog. 2012; 8:e1002843. PMID: 22876182. doi: 10.1371/journal.ppat. 1002843
9. Khodaverdian V, Pesho M, Truitt B, Bollinger L, Patel P, Nithianantham S, et al. Discovery of antiviru-lence agents against methicillin-resistant Staphylococcus aureus. Antimicrobial agents and chemotherapy. 2013; 57: 3645-3652. PMID: 23689713. doi: 10.1128/AAC.00269-13
10. Novick RP, Projan SJ, Kornblum J, Ross HF, Ji G, Kreiswirth B, et al. The agr P2 operon: an autocata-lytic sensory transduction system in Staphylococcus aureus. Mol Gen Genet. 1995; 248: 446-458. PMID: 7565609.
11. Smith K, Gould KA, Ramage G, Gemmell CG, Hinds J, Lang S. Influence of tigecycline on expression of virulence factors in biofilm-associated cells of methicillin-resistant Staphylococcus aureus. Antimicrobial agents and chemotherapy. 2010; 54: 380-387. PMID: 19858261. doi: 10.1128/AAC.00155-09
12. Cassat J, Dunman PM, Murphy E, Projan SJ, Beenken KE, Palm KJ, et al. Transcriptional profiling of a Staphylococcus aureus clinical isolate and its isogenic agr and sarA mutants reveals global differences in comparison to the laboratory strain RN6390. Microbiology (Reading, England). 2006; 152: 3075-3090. PMID: 17005987.
13. Blickwede M, Valentin-Weigand P, Rohde M, Schwarz S. Effects of subinhibitory concentrations of flor-fenicolon morphology, growth, and viability of Staphylococcus aureus. J Vet Med B Infect Dis Vet Public Health. 2004; 51: 293-296. PMID: 15458493.
14. Braga PC, Dal Sasso M, Maci S. Cefodizime: effects of sub-inhibitory concentrations on adhesiveness and bacterial morphology of Staphylococcus aureus and Escherichia coli: comparison with cefotaxime and ceftriaxone. J Antimicrob Chemother. 1997; 39: 79-84. PMID: 9044031.
15. Rachid S, Ohlsen K, Witte W, Hacker J, Ziebuhr W. Effect of subinhibitory antibiotic concentrations on polysaccharide intercellular adhesin expression in biofilm-forming Staphylococcus epidermidis. Antimicrobial agents and chemotherapy. 2000; 44: 3357-3363. PMID: 11083640.
16. Kaplan JB, Jabbouri S, Sadovskaya I. Extracellular DNA-dependentbiofilm formation by Staphylococcus epidermidis RP62A in response to subminimal inhibitory concentrations of antibiotics. Res Microbiol. 2011; 162: 535-341. PMID: 21402153. doi: 10.1016/j.resmic.2011.03.008
17. Kaplan JB, Izano EA, Gopal P, Karwacki MT, Kim S, Bose JL, et al. Low levels of beta-lactam antibiotics induce extracellular DNA release and biofilm formation in Staphylococcus aureus. MBio. 2012; 3: e00198-12. PMID: 22851659. doi: 10.1128/mBio.00198-12
18. Gomes DL, Peixoto RS, Barbosa EA, Napoleao F, Sabbadini PS, dos Santos KR, et al. Sub MICs of penicillin and erythromycin enhance biofilm formation and hydrophobicity of Corynebacterium diphther-iae strains. J Med Microbiol. 2013; 62: 754-760. PMID: 23449875. doi: 10.1099/jmm.0.052373-0
19. Frank KL, Reichert EJ, Piper KE, Patel R. In vitro effects of antimicrobial agents on planktonic and biofilm forms of Staphylococcus lugdunensis clinical isolates. Antimicrobial agents and chemotherapy. 2007; 51: 888-895. PMID: 17158933.
20. Davies J, Spiegelman GB, Yim G. The world of subinhibitory antibiotic concentrations. Curr Opin Microbiol. 2006; 9: 445-453. PMID: 16942902.
21. Villegas-Estrada A, Lee M, Hesek D, Vakulenko SB, Mobashery S. Co-opting the cell wall in fighting methicillin-resistant Staphylococcus aureus: potent inhibition of PBP 2a by two anti-MRSA beta-lactam antibiotics. J Am Chem Soc. 2008; 130: 9212-9213. PMID: 18582062. doi: 10.1021/ja8029448
22. Werth BJ, Barber KE, Ireland CE, Rybak MJ. Evaluation of ceftaroline, vancomycin, daptomycin, orcef-taroline plus daptomycin against daptomycin-nonsusceptible methicillin-resistant Staphylococcus aureus in an in vitro pharmacokinetic/pharmacodynamic model of simulated endocardial vegetations. Antimicrobial agents and chemotherapy. 2014; 58: 3177-3181. PMID: 24663016. doi: 10.1128/AAC. 00088-14
23. Saravolatz L, Pawlak J, Johnson L. In vitro activity of ceftaroline against community-associated methicillin-resistant, vancomycin-intermediate, vancomycin-resistant, and daptomycin-nonsusceptible Staphylococcus aureus isolates. Antimicrobial agents and chemotherapy. 2010; 54: 3027-3030. PMID: 20404122. doi: 10.1128/AAC.01516-09
24. Biek D, Critchley IA, Riccobene TA, Thye DA. Ceftaroline fosamil: a novel broad-spectrum cephalosporin with expanded anti-Gram-positive activity. J Antimicrob Chemother. 2010; 65: iv9-16. PMID: 21115457. doi: 10.1093/jac/dkq251
25. Long SW, Olsen RJ, Mehta SC, Palzkill T, Cernoch PL, Perez KK, et al. PBP2a mutations causing high-level Ceftaroline resistance in clinical methicillin-resistant Staphylococcus aureus isolates. Antimicrobial agents and chemotherapy. 2014; 58: 6668-6674. PMID: 25155594. doi: 10.1128/AAC.03622-14
26. Institute Ca LS. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard, 9th ed. CLSI document M7-A9. Clinical and Laboratory Standards Institute, Wayne, PA. 2012.
27. O'Toole GA, Kolter R. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol Microbiol. 1998; 28: 449-461. PMID: 9632250.
28. Goerke C, Campana S, Bayer MG, Doring G, Botzenhart K, Wolz C. Direct quantitative transcript analysis of the agr regulon of Staphylococcus aureus during human infection in comparison to the expression profile in vitro. Infect Immun. 2000; 68:1304-1311. PMID: 10678942.
29. Pozzi C, Waters EM, Rudkin JK, Schaeffer CR, Lohan AJ, Tong P, et al. Methicillin resistance alters the biofilm phenotype and attenuates virulence in Staphylococcus aureus device-associated infections. PloS Pathog. 2012; 8: e1002626. PMID: 22496652. doi: 10.1371/journal.ppat. 1002626
30. Valle J, Toledo-Arana A, Berasain C, Ghigo JM, Amorena B, Penades JR, et al. Sar Aand notsigmaB is essential for biofilm development by Staphylococcus aureus. Mol Microbiol. 2003; 48:1075-1087. PMID: 12753197.
31. Saravolatz LD, Stein GE, Johnson LB. Ceftaroline: a novel cephalosporin with activity against methicil-lin-resistantStaphylococcusaureus. Clin Infect Dis. 2011; 52:1156-1163. PMID: 21467022. doi: 10. 1093/cid/cir147
32. Pottinger PS. Methicillin-resistant Staphylococcus aureus infections. Med Clin North Am. 2013; 97: 601-619. PMID: 23809716. doi: 10.1016/j.mcna.2013.02.005
33. Odenholt I. Pharmacodynamic effects of subinhibitory antibiotic concentrations. Int J Antimicrob Agents. 2001; 17:1-8. PMID: 11137642.
34. Subrt N, Mesak LR, Davies J. Modulation of virulence gene expression by cell wall active antibiotics in Staphylococcus aureus. J Antimicrob Chemother. 2011; 66: 979-984. PMID: 21393149. doi: 10.1093/jac/dkr043
35. Kaplan JB. Antibiotic-induced biofilm formation. Int J Artif Organs. 2011; 34:737-751. PMID: 22094552. doi: 10.5301/ijao.5000027
36. Zhou X, Halladin DK, Rojas ER, Koslover EF, Lee TK, Huang KC, et al. Bacterial division. Mechanical crack propagation drives millisecond daughter cell separation in Staphylococcus aureus. Science. 2015; 348: 574-578. PMID: 25931560. doi: 10.1126/science.aaa1511
37. Gil C, Solano C, Burgui S, Latasa C, Garcia B, Toledo-Arana A, et al. Biofilm matrixexoproteins induce a protective immune response against Staphylococcus aureus biofilm infection. Infect Immun. 2014; 82:1017-1029. PMID: 24343648. doi: 10.1128/IAI.01419-13
38. Landini G, Riccobono E, Giani T, Arena F, Rossolini GM, Pallecchi L. Bactericidal activity of ceftaroline against mature Staphylococcus aureus biofilms. Int J Antimicrob Agents. 2015; 45: 551-553. PMID: 25661754. doi: 10.1016/j.ijantimicag.2015.01.001
39. Suci PA, Mittelman MW, Yu FP, Geesey GG. Investigation of ciprofloxacin penetration into Pseudomonas aeruginosa biofilms. Antimicrobial agents and chemotherapy. 1994; 38:2125-2133. PMID: 7811031.
40. Singh R, Ray P, Das A, Sharma M. Penetration of antibiotics through Staphylococcus aureus and Staphylococcus epidermidis biofilms. J Antimicrob Chemother. 2010; 65:1955-1958. PMID: 20615927. doi: 10.1093/jac/dkq257
41. Brooks JL, Jefferson KK. Staphylococcal biofilms: questforthe magic bullet. Adv Appl Microbiol. 2012; 81: 63-87. PMID: 22958527. doi: 10.1016/B978-0-12-394382-8.00002-2
42. Donlan RM, Costerton JW. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev. 2002; 15:167-193. PMID: 11932229.
43. Joo HS, Chan JL, Cheung GY, Otto M. Subinhibitory concentrations of protein synthesis-inhibiting antibiotics promote increased expression of the agr virulence regulator and production of phenol-soluble modulin cytolysins in community-associated methicillin-resistant Staphylococcus aureus. Antimicrobial agents and chemotherapy. 2010; 54: 4942-4944. PMID: 20713669. doi: 10.1128/AAC.00064-10
44. Barber KE, Werth BJ, McRoberts JP, Rybak MJ. A novel approach utilizing biofilm time-kill curves to assess the bactericidal activity of ceftaroline combinations against biofilm-producing methicillin-resis-tant Staphylococcus aureus. Antimicrobial agents and chemotherapy. 2014; 58: 2989-2992. PMID: 24614378. doi: 10.1128/AAC.02764-13