Sequential Evolution of Vancomycin-Intermediate Resistance Alters Virulence in Staphylococcus aureus: Pharmacokinetic/Pharmacodynamic Targets for Vancomycin Exposure

Antimicrobial Agents and Chemotherapy

Volumn 60, Issue 3, 2016, Pages 1584-1591

  Lenhard, Justin R ^a   Brown, Tanya ^a,e   Rybak, Michael J ^b   Meaney, Calvin J ^a   Norgard, Nicholas B ^a   Bulman, Zackery P ^a   Brazeau, Daniel A ^d   Gill, Steven R ^c   Tsuji, Brian T ^a  

^a UNIVERSITY AT BUFFALO   (United States)

^b WAYNE STATE UNIVERSITY   (United States)

^c UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^d UNIVERSITY OF NEW ENGLAND   (United States)

^e FLORIDA INTERNATIONAL UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CIPROFLOXACIN; DAPTOMYCIN; GENTAMICIN; LEVOFLOXACIN; NAFCILLIN; RIFAMPICIN; TELAVANCIN; VANCOMYCIN; AMINOGLYCOSIDE; ANTIINFECTIVE AGENT; BACTERIAL RNA; RNAIII, STAPHYLOCOCCUS AUREUS;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC THERAPY; ARTICLE; BACTERIAL COUNT; BACTERIAL GROWTH; BACTERIAL VIRULENCE; BACTERICIDAL ACTIVITY; COLONY FORMING UNIT; CONTROLLED STUDY; DOSE RESPONSE; DRUG DOSE INCREASE; DRUG EXPOSURE; GALLERIA MELLONELLA; GENE EXPRESSION; HOST PATHOGEN INTERACTION; HUMAN; IN VITRO STUDY; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS INFECTION; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PRIORITY JOURNAL; VANCOMYCIN INTERMEDIATE STAPHYLOCOCCUS AUREUS; ANIMAL; BIOSYNTHESIS; DRUG EFFECTS; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; MOTH; PATHOGENICITY; STAPHYLOCOCCAL INFECTIONS;

AMINOGLYCOSIDES; ANIMALS; ANTI-BACTERIAL AGENTS; DAPTOMYCIN; HOST-PATHOGEN INTERACTIONS; HUMANS; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIAL SENSITIVITY TESTS; MOTHS; RNA, BACTERIAL; STAPHYLOCOCCAL INFECTIONS; VANCOMYCIN; VANCOMYCIN RESISTANCE;

EID: 84960452494     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.02657-15     Document Type: Article

References (43)

1. Lowy FD. 1998. Staphylococcus aureus infections. N Engl J Med 339:520-532. http://dx.doi.org/10.1056/NEJM199808203390806.
2. Hanaki H, Kuwahara-Arai K, Boyle-Vavra S, Daum RS, Labischinski H, Hiramatsu K. 1998. Activated cell wall synthesis is associated with vancomycin resistance in methicillin-resistant Staphylococcus aureus clinical strains Mu3 and Mu50. J Antimicrob Chemother 42:199-209. http://dx.doi.org/10.1093/jac/42.2.199.
3. Hanaki H, Labischinski H, Inaba Y, Kondo N, Murakami H, Hiramatsu K. 1998. Increase in glutamine-non-amidated muropeptides in the peptidoglycan of vancomycin-resistant Staphylococcus aureus strain Mu50. J Antimicrob Chemother 42:315-320. http://dx.doi.org/10.1093/jac/42.3.315.
4. Hiramatsu K, Hanaki H, Ino T, Yabuta K, Oguri T, Tenover FC. 1997. Methicillin-resistant Staphylococcus aureus clinical strain with reduced vancomycin susceptibility. J Antimicrob Chemother 40:135-136. http://dx.doi.org/10.1093/jac/40.1.135.
5. Sieradzki K, Tomasz A. 2003. Alterations of cell wall structure and metabolism accompany reduced susceptibility to vancomycin in an isogenic series of clinical isolates of Staphylococcus aureus. J Bacteriol 185:7103-7110. http://dx.doi.org/10.1128/JB.185.24.7103-7110.2003.
6. Tsuji BT, von Eiff C, Kelchlin PA, Forrest A, Smith PF. 2008. Attenuated vancomycin bactericidal activity against Staphylococcus aureus hemB mutants expressing the small-colony-variant phenotype. Antimicrob Agents Chemother 52:1533-1537. http://dx.doi.org/10.1128/AAC.01254-07.
7. Alam MT, Petit RA, III, Crispell EK, Thornton TA, Conneely KN, Jiang Y, Satola SW, Read TD. 2014. Dissecting vancomycin-intermediate resistance in Staphylococcus aureus using genome-wide association. Genome Biol Evol 6:1174-1185. http://dx.doi.org/10.1093/gbe/evu092.
8. Vidaillac C, Gardete S, Tewhey R, Sakoulas G, Kaatz GW, Rose WE, Tomasz A, Rybak MJ. 2013. Alternative mutational pathways to intermediate resistance to vancomycin in methicillin-resistant Staphylococcus aureus. J Infect Dis 208:67-74. http://dx.doi.org/10.1093/infdis/jit127.
9. Howden BP, Smith DJ, Mansell A, Johnson PD, Ward PB, Stinear TP, Davies JK. 2008. Different bacterial gene expression patterns and attenuated host immune responses are associated with the evolution of low-level vancomycin resistance during persistent methicillin-resistant Staphylococcus aureus bacteraemia. BMC Microbiol 8:39. http://dx.doi.org/10.1186/1471-2180-8-39.
10. Mwangi MM, Wu SW, Zhou Y, Sieradzki K, De Lencastre H, Richardson P, Bruce D, Rubin E, Myers E, Siggia ED, Tomasz A. 2007. Tracking the in vivo evolution of multidrug resistance in Staphylococcus aureus by whole-genome sequencing. Proc Natl Acad SciUSA104:9451-9456. http://dx.doi.org/10.1073/pnas.0609839104.
11. Zhang S, Sun X, Chang W, Dai Y, Ma X. 2015. Systematic review and meta-analysis of the epidemiology of vancomycin-intermediate and heterogeneous vancomycin-intermediate Staphylococcus aureus isolates. PLoS One 10:e0136082. http://dx.doi.org/10.1371/journal.pone.0136082.
12. Novick RP. 2003. Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol Microbiol 48:1429-1449. http://dx.doi.org/10.1046/j.1365-2958.2003.03526.x.
13. Lyon GJ, Wright JS, Muir TW, Novick RP. 2002. Key determinants of receptor activation in the agr autoinducing peptides of Staphylococcus aureus. Biochemistry 41:10095-10104. http://dx.doi.org/10.1021/bi 026049u.
14. Ji G, Beavis R, Novick RP. 1997. Bacterial interference caused by autoinducing peptide variants. Science 276:2027-2030. http://dx.doi.org/10.1126/science.276.5321.2027.
15. Moise-Broder PA, Sakoulas G, Eliopoulos GM, Schentag JJ, Forrest A, Moellering RC, Jr. 2004. Accessory gene regulator group II polymorphism in methicillin-resistant Staphylococcus aureus is predictive of failure of vancomycin therapy. Clin Infect Dis 38:1700-1705. http://dx.doi.org/10.1086/421092.
16. Tsuji BT, Rybak MJ, Lau KL, Sakoulas G. 2007. Evaluation of accessory gene regulator (agr) group and function in the proclivity towards vancomycin intermediate resistance in Staphylococcus aureus. Antimicrob Agents Chemother 51:1089-1091. http://dx.doi.org/10.1128/AAC.00671-06.
17. Sakoulas G, Eliopoulos GM, Moellering RC, Jr, Novick RP, Venkataraman L, Wennersten C, DeGirolami PC, Schwaber MJ, Gold HS. 2003. Staphylococcus aureus accessory gene regulator (agr) group II: Is there a relationship to the development of intermediate-level glycopeptide resistance? J Infect Dis 187:929-938. http://dx.doi.org/10.1086/368128.
18. Diep BA, Gill SR, Chang RF, Phan TH, Chen JH, Davidson MG, Lin F, Lin J, Carleton HA, Mongodin EF, Sensabaugh GF, Perdreau-Remington F. 2006. Complete genome sequence of USA300, an epidemic clone of community-acquired methicillin-resistant Staphylococcus aureus. Lancet 367:731-739. http://dx.doi.org/10.1016/S0140-6736(06)68231-7.
19. Baba T, Takeuchi F, Kuroda M, Yuzawa H, Aoki K, Oguchi A, Nagai Y, Iwama N, Asano K, Naimi T, Kuroda H, Cui L, Yamamoto K, Hiramatsu K. 2002. Genome and virulence determinants of high virulence community-acquired MRSA. Lancet 359:1819-1827. http://dx.doi.org/10.1016/S0140-6736(02)08713-5.
20. Holden MT, Feil EJ, Lindsay JA, Peacock SJ, Day NP, Enright MC, Foster TJ, Moore CE, Hurst L, Atkin R, Barron A, Bason N, Bentley SD, Chillingworth C, Chillingworth T, Churcher C, Clark L, Corton C, Cronin A, Doggett J, Dowd L, Feltwell T, Hance Z, Harris B, Hauser H, Holroyd S, Jagels K, James KD, Lennard N, Line A, Mayes R, Moule S, Mungall K, Ormond D, Quail MA, Rabbinowitsch E, Rutherford K, Sanders M, Sharp S, Simmonds M, Stevens K, Whitehead S, Barrell BG, Spratt BG, Parkhill J. 2004. Complete genomes of two clinical Staphylococcus aureus strains: Evidence for the rapid evolution of virulence and drug resistance. Proc Natl Acad Sci U S A 101:9786-9791. http://dx.doi.org/10.1073/pnas.0402521101.
21. Gumbo T, Louie A, Deziel MR, Parsons LM, Salfinger M, Drusano GL. 2004. Selection of a moxifloxacin dose that suppresses drug resistance in Mycobacterium tuberculosis, by use of an in vitro pharmacodynamic infection model and mathematical modeling. J Infect Dis 190:1642-1651. http://dx.doi.org/10.1086/424849.
22. Tsuji BT, Brown T, Parasrampuria R, Brazeau DA, Forrest A, Kelchlin PA, Holden PN, Peloquin CA, Hanna D, Bulitta JB. 2012. Front-loaded linezolid regimens result in increased killing and suppression of the accessory gene regulator system of Staphylococcus aureus. Antimicrob Agents Chemother 56:3712-3719. http://dx.doi.org/10.1128/AAC.05453-11.
23. Peleg AY, Jara S, Monga D, Eliopoulos GM, Moellering RC, Jr, Mylonakis E. 2009. Galleria mellonella as a model system to study Acinetobacter baumannii pathogenesis and therapeutics. Antimicrob Agents Chemother 53:2605-2609. http://dx.doi.org/10.1128/AAC.01533-08.
24. Bulman ZP, Sutton MD, Ly NS, Bulitta JB, Holden PN, Nation RL, Li J, Tsuji BT. 2015. Emergence of polymyxin B resistance influences pathogenicity in Pseudomonas aeruginosa mutators. Antimicrob Agents Chemother 59:4343-4346. http://dx.doi.org/10.1128/AAC.04629-14.
25. Lenhard JR, von Eiff C, Hong IS, Holden PN, Bear MD, Suen A, Bulman ZP, Tsuji BT. 2015. Evolution of Staphylococcus aureus under vancomycin selective pressure: The role of the small-colony variant phenotype. Antimicrob Agents Chemother 59:1347-1351. http://dx.doi.org/10.1128/AAC.04508-14.
26. Casapao AM, Leonard SN, Davis SL, Lodise TP, Patel N, Goff DA, Laplante KL, Potoski BA, Rybak MJ. 2013. Clinical outcomes in patients with heterogeneous vancomycin-intermediate Staphylococcus aureus (hVISA) bloodstream infection. Antimicrob Agents Chemother http://dx.doi.org/10.1128/aac.00380-13.
27. Casapao AM, Davis SL, McRoberts JP, Lagnf AM, Patel S, Kullar R, Levine DP, Rybak MJ. 2014. Evaluation of vancomycin population susceptibility analysis profile as a predictor of outcomes for patients with infective endocarditis due to methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 58:4636-4641. http://dx.doi.org/10.1128/AAC.02820-13.
28. De Vriese AS, Vandecasteele SJ. 2014. Vancomycin: The tale of the vanquisher and the pyrrhic victory. Peritoneal Dial Int 34:154-161.
29. Fong RK, Low J, Koh TH, Kurup A. 2009. Clinical features and treatment outcomes of vancomycin-intermediate Staphylococcus aureus (VISA) and heteroresistant vancomycin-intermediate Staphylococcus aureus (hVISA) in a tertiary care institution in Singapore. Eur J Clin Microbiol Infect Dis 28:983-987. http://dx.doi.org/10.1007/s10096-009-0741-5.
30. Moise PA, Schentag JJ. 2000. Vancomycin treatment failures in Staphylococcus aureus lower respiratory tract infections. Int J Antimicrob Agents 16(Suppl 1):S31-S34.
31. Rybak M, Lomaestro B, Rotschafer JC, Moellering R, Jr, Craig W, Billeter M, Dalovisio JR, Levine DP. 2009. Therapeutic monitoring of vancomycin in adult patients: A consensus review of the American Society of Health-System Pharmacists, the Infectious Diseases Society of America, and the Society of Infectious Diseases Pharmacists. Am J Health Syst Pharm 66:82-98. http://dx.doi.org/10.2146/ajhp080434.
32. Tam VH, Louie A, Deziel MR, Liu W, Drusano GL. 2007. The relationship between quinolone exposures and resistance amplification is characterized by an inverted U: A new paradigm for optimizing pharmacodynamics to counterselect resistance. Antimicrob Agents Chemother 51: 744-747. http://dx.doi.org/10.1128/AAC.00334-06.
33. Tsuji BT, Rybak MJ, Cheung CM, Amjad M, Kaatz GW. 2007. Community-and health care-associated methicillin-resistant Staphylococcus aureus: A comparison of molecular epidemiology and antimicrobial activities of various agents. Diagn Microbiol Infect Dis 58:41-47. http://dx.doi.org/10.1016/j.diagmicrobio.2006.10.021.
34. Viedma E, Sanz F, Orellana MA, San Juan R, Aguado JM, Otero JR, Chaves F. 2014. Relationship between agr dysfunction and reduced vancomycin susceptibility in methicillin-susceptible Staphylococcus aureus causing bacteraemia. J Antimicrob Chemother 69:51-58. http://dx.doi.org/10.1093/jac/dkt337.
35. Rudkin JK, Edwards AM, Bowden MG, Brown EL, Pozzi C, Waters EM, Chan WC, Williams P, O'Gara JP, Massey RC. 2012. Methicillin resistance reduces the virulence of healthcare-associated methicillin-resistant Staphylococcus aureus by interfering with the agr quorum sensing system. J Infect Dis 205:798-806. http://dx.doi.org/10.1093/infdis/jir845.
36. Gardete S, Kim C, Hartmann BM, Mwangi M, Roux CM, Dunman PM, Chambers HF, Tomasz A. 2012. Genetic pathway in acquisition and loss of vancomycin resistance in a methicillin-resistant Staphylococcus aureus (MRSA) strain of clonal type USA300. PLoS Pathog 8:e1002505. http://dx.doi.org/10.1371/journal.ppat.1002505.
37. Craven RR, Gao X, Allen IC, Gris D, Bubeck Wardenburg J, McElvania-Tekippe E, Ting JP, Duncan JA. 2009. Staphylococcus aureus alphahemolysin activates the NLRP3-inflammasome in human and mouse monocytic cells. PLoS One 4:e7446. http://dx.doi.org/10.1371/journal.pone.0007446.
38. Onogawa T. 2002. Staphylococcal alpha-toxin synergistically enhances inflammation caused by bacterial components. FEMS Immunol Med Microbiol 33:15-21. http://dx.doi.org/10.1016/S0928-8244(01)00308-X.
39. Proctor RA, von Eiff C, Kahl BC, Becker K, McNamara P, Herrmann M, Peters G. 2006. Small colony variants: A pathogenic form of bacteria that facilitates persistent and recurrent infections. Nat Rev Microbiol 4:295-305. http://dx.doi.org/10.1038/nrmicro1384.
40. Rose WE, Leonard SN, Rossi KL, Kaatz GW, Rybak MJ. 2009. Impact of inoculum size and heterogeneous vancomycin-intermediate Staphylococcus aureus (hVISA) on vancomycin activity and emergence of VISA in an in vitro pharmacodynamic model. Antimicrob Agents Chemother 53: 805-807. http://dx.doi.org/10.1128/AAC.01009-08.
41. Lee DG, Murakami Y, Andes DR, Craig WA. 2013. Inoculum effects of ceftobiprole, daptomycin, linezolid, and vancomycin with Staphylococcus aureus and Streptococcus pneumoniae at inocula of 105 and 107 CFU injected into opposite thighs of neutropenic mice. Antimicrob Agents Chemother 57:1434-1441. http://dx.doi.org/10.1128/AAC.00362-12.
42. Lodise TP, Lomaestro B, Graves J, Drusano GL. 2008. Larger vancomycin doses (at least four grams per day) are associated with an increased incidence of nephrotoxicity. Antimicrob Agents Chemother 52:1330-1336. http://dx.doi.org/10.1128/AAC.01602-07.
43. Harigaya Y, Bulitta JB, Forrest A, Sakoulas G, Lesse AJ, Mylotte JM, Tsuji BT. 2009. Pharmacodynamics of vancomycin at simulated epithelial lining fluid concentrations against methicillin-resistant Staphylococcus aureus (MRSA): Implications for dosing in MRSA pneumonia. Antimicrob Agents Chemother 53:3894-3901. http://dx.doi.org/10.1128/AAC.01585-08.