Vancomycin tolerance in Gram-positive cocci

Environmental Microbiology Reports

Volumn 3, Issue 6, 2011, Pages 640-650

  Moscoso, Miriam ^a   Domenech, Mirian ^a   García, Ernesto ^a  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ENTEROCOCCUS; ENTEROCOCCUS FAECALIS; POSIBACTERIA; STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS; STREPTOCOCCUS PNEUMONIAE;

EID: 84859839143     PISSN: None     EISSN: 17582229     Source Type: Journal    
DOI: 10.1111/j.1758-2229.2011.00254.x     Document Type: Review

References (100)

1. Abranches, J., Martinez, A.R., Kajfasz, J.K., Chavez, V., Garsin, D.A., and Lemos, J.A. (2009) The molecular alarmone (p)ppGpp mediates stress responses, vancomycin tolerance, and virulence in Enterococcus faecalis. J Bacteriol 191: 2248-2256.
2. Appleman, M.D., and Citron, D.M. (2010) Efficacy of vancomycin and daptomycin against Staphylococcus aureus isolates collected over 29 years. Diagn Microbiol Infect Dis 66: 441-444.
3. van Asselt, G.J., Mouton, R.P., and van Boven, C.P.A. (1996) A proposed standard for MIC-MBC laboratory techniques to detect penicillin tolerance in group A streptococci. Eur J Clin Microb Infect Dis 15: 182-183.
4. Bayles, K.W. (2007) The biological role of death and lysis in biofilm development. Nat Rev Microbiol 5: 721-726.
5. Bizzini, A., Zhao, C., Auffray, Y., and Hartke, A. (2009) The Enterococcus faecalis superoxide dismutase is essential for its tolerance to vancomycin and penicillin. J Antimicrob Chemother 64: 1196-1202.
6. Boost, M.V., Ko, W.M., and O'Donoghue, M.M. (2003) Penicillin and vancomycin tolerance among clinical isolates of Streptococcus pneumoniae in Hong Kong. Hong Kong Med J 9: 415-418.
7. Bouza, E., and Burillo, A. (2010) Oritavancin: a novel lipoglycopeptide active against Gram-positive pathogens including multiresistant strains. Int J Antimicrob Agents 36: 401-407.
8. Cargill, J.S., and Upton, M. (2009) Low concentrations of vancomycin stimulate biofilm formation in some clinical isolates of Staphylococcus epidermidis. J Clin Pathol 62: 1112-1116.
9. CLSI (1999) Methods for determining bactericidal activity of antimicrobial agents. Approved guideline. Document M26-A. [WWW document] URL (accessed on 16 November 2010).
10. Costa, A., Henriques, M., Oliveira, R., and Azeredo, J. (2009) The role of polysaccharide intercellular adhesin (PIA) in Staphylococcus epidermidis adhesion to host tissues and subsequent antibiotic tolerance. Eur J Clin Microb Infect Dis 28: 623-629.
11. Cunha, B.A., Mickail, N., and Eisenstein, L. (2007) E. faecalis vancomycin-sensitive enterococcal bacteremia unresponsive to a vancomycin tolerant strain successfully treated with high-dose daptomycin. Heart Lung 36: 456-461.
12. Chakraborty, S.P., Sahu, S.K., Mahapatra, S.K., Santra, S., Bal, M., Roy, S., and Pramanik, P. (2010) Nanoconjugated vancomycin: new opportunities for the development of anti-VRSA agents. Nanotechnology 21: 105103.
13. Dalebroux, Z.D., Svensson, S.L., Gaynor, E.C., and Swanson, M.S. (2010) ppGpp conjures bacterial virulence. Microbiol Mol Biol Rev 74: 171-199.
14. Dörr, T., Vulić, M., and Lewis, K. (2010) Ciprofloxacin causes persister formation by inducing the TisB toxin in Escherichia coli. PLoS Biol 8: e1000317.
15. von Eiff, C., Peters, G., and Heilmann, C. (2002) Pathogenesis of infections due to coagulase-negative staphylococci. Lancet Infect Dis 2: 677-685.
16. Eldholm, V., Gutt, B., Johnsborg, O., Brückner, R., Maurer, P., Hakenbeck, R., etal. (2010) The pneumococcal cell envelope stress-sensing system LiaFSR is activated by murein hydrolases and lipid II-interacting antibiotics. J Bacteriol 192: 1761-1773.
17. Eliopoulos, G.M. (2009) Microbiology of drugs for treating multiply drug-resistant Gram-positive bacteria. J Infect 59: S17-S24.
18. EUCAST (2010) Breakpoint tables for interpretation of MICs and zone diameters. V 1.1, April 2010. [WWW document] URL (accessed on 16 November 2010).
19. Fernebro, J., Andersson, I., Sublett, J., Morfeldt, E., Novak, R., Tuomanen, E., etal. (2004) Capsular expression in Streptococcus pneumoniae negatively affects spontaneous and antibiotic-induced lysis and contributes to antibiotic tolerance. J Infect Dis 189: 328-338.
20. Filipe, S.R., and Tomasz, A. (2000) Inhibition of the expression of penicillin resistance in Streptococcus pneumoniae by inactivation of cell wall muropeptide branching genes. Proc Natl Acad Sci USA 97: 4891-4896.
21. Filipe, S.R., Severina, E., and Tomasz, A. (2002) The murMN operon: a functional link between antibiotic resistance and antibiotic tolerance in Streptococcus pneumoniae. Proc Natl Acad Sci USA 99: 1550-1555.
22. Fisher, K., and Phillips, C. (2009) The ecology, epidemiology and virulence of Enterococcus. Microbiology 155: 1749-1757.
23. Frank, K.L., del Pozo, J.L., and Patel, R. (2008) From clinical microbiology to infection pathogenesis: how daring to be different works for Staphylococcus lugdunensis. Clin Microbiol Rev 21: 111-133.
24. Fritsche, T.R., Rhomberg, P.R., Sader, H.S., and Jones, R.N. (2008) In vitro activity of omiganan pentahydrochloride tested against vancomycin-tolerant, -intermediate, and -resistant Staphylococcus aureus. Diagn Microbiol Infect Dis 60: 399-403.
25. Fung, D.K.C., Chan, E.W.C., Chin, M.L., and Chan, R.C.Y. (2010) Delineation of a bacterial starvation stress response network which can mediate antibiotic tolerance development. Antimicrob Agents Chemother 54: 1082-1093.
26. Gao, W., Chua, K., Davies, J.K., Newton, H.J., Seemann, T., Harrison, P.F., etal. (2010) Two novel point mutations in clinical Staphylococcus aureus reduce linezolid susceptibility and switch on the stringent response to promote persistent infection. PLoS Pathog 6: e1000944.
27. Geiger, T., Goerke, C., Fritz, M., Schäfer, T., Ohlsen, K., Liebeke, M., etal. (2010) Role of the (p)ppGpp synthase RSH, a RelA/SpoT homolog, in stringent response and virulence of Staphylococcus aureus. Infect Immun 78: 1873-1883.
28. Gillis, L.M., White, H.D., Whitehurst, A., and Sullivan, D.C. (2005) Vancomycin-tolerance among clinical isolates of Streptococcus pneumoniae in Mississippi during 1999-2001. Am J Med Sci 330: 65-68.
29. Gotoh, Y., Eguchi, Y., Watanabe, T., Okamoto, S., Doi, A., and Utsumi, R. (2010) Two-component signal transduction as potential drug targets in pathogenic bacteria. Curr Opin Microbiol 13: 232-239.
30. Guskey, M.T., and Tsuji, B.T. (2010) A comparative review of the lipoglycopeptides: oritavancin, dalbavancin, and telavancin. Pharmacotherapy 30: 80-94.
31. Haas, W., Sublett, J., Kaushal, D., and Tuomanen, E.I. (2004) Revising the role of the pneumococcal vex-vncRS locus in vancomycin tolerance. J Bacteriol 186: 8463-8471.
32. Haas, W., Kaushal, D., Sublett, J., Obert, C., and Tuomanen, E.I. (2005) Vancomycin stress response in a sensitive and a tolerant strain of Streptococcus pneumoniae. J Bacteriol 187: 8205-8210.
33. Hegstad, K., Mikalsen, T., Coque, T.M., Werner, G., and Sundsfjord, A. (2010) Mobile genetic elements and their contribution to the emergence of antimicrobial resistant Enterococcus faecalis and Enterococcus faecium. Clin Microbiol Infect 16: 541-554.
34. Henriques Normark, B., Novak, R., Örtqvist, Å., Källenius, G., Tuomanen, E., and Normark, S. (2001) Clinical isolates of Streptococcus pneumoniae that exhibit tolerance of vancomycin. Clin Infect Dis 32: 552-558.
35. Hidalgo, M., Castañeda, E., and Arias, C.A. (2003) Tolerance to vancomycin in a multiresistant, Colombian isolate of Streptococcus pneumoniae. J Antimicrob Chemother 52: 300-302.
36. Horne, D., and Tomasz, A. (1977) Tolerant tesponse of Streptococcus sanguis to beta-lactams and other cell wall inhibitors. Antimicrob Agents Chemother 11: 888-896.
37. Howden, B.P., Davies, J.K., Johnson, P.D.R., Stinear, T.P., and Grayson, M.L. (2010) Reduced vancomycin susceptibility in Staphylococcus aureus, including vancomycin-intermediate and heterogeneous vancomycin-intermediate strains: resistance mechanisms, laboratory detection, and clinical implications. Clin Microbiol Rev 23: 99-139.
38. Hu, Y., Shamaei-Tousi, A., Liu, Y., and Coates, A. (2010) A new approach for the discovery of antibiotics by targeting non-multiplying bacteria: a novel topical antibiotic for Staphylococcal infections. PLoS ONE 5: e11818.
39. Jõers, A., Kaldalu, N., and Tenson, T. (2010) The frequency of persisters in Escherichia coli reflects the kinetics of awakening from dormancy. J Bacteriol 192: 3379-3384.
40. Jones, R.N. (2010) Microbial etiologies of hospital-acquired bacterial pneumonia and ventilator-associated bacterial pneumonia. Clin Infect Dis 51: S81-S87.
41. Jordan, S., Hutchings, M.I., and Mascher, T. (2008) Cell envelope stress response in Gram-positive bacteria. FEMS Microbiol Rev 32: 107-146.
42. Kallen, A.J., Mu, Y., Bulens, S., Reingold, A., Petit, S., Gershman, K., etal. (2010) Health care-associated invasive MRSA infections, 2005-2008. JAMA 304: 641-647.
43. Spn in stringent response, global regulation and virulence of serotype 2 Streptococcus pneumoniae D39. Mol Microbiol 72: 590-611.
44. Keren, I., Kaldalu, N., Spoering, A., Wang, Y., and Lewis, K. (2004) Persister cells and tolerance to antimicrobials. FEMS Microbiol Lett 230: 13-18.
45. Koehl, J.L., Muthaiyan, A., Jayaswal, R.K., Ehlert, K., Labischinski, H., and Wilkinson, B.J. (2004) Cell wall composition and decreased autolytic activity and lysostaphin susceptibility of glycopeptide-intermediate Staphylococcus aureus. Antimicrob Agents Chemother 48: 3749-3757.
46. Kohanski, M.A., Dwyer, D.J., Hayete, B., Lawrence, C.A., and Collins, J.J. (2007) A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130: 797-810.
47. Lauderdale, K.J., Boles, B.R., Cheung, A.L., and Horswill, A.R. (2009) Interconnections between Sigma B, agr, and proteolytic activity in Staphylococcus aureus biofilm maturation. Infect Immun 77: 1623-1635.
48. Levin, B.R., and Rozen, D.E. (2006) Non-inherited antibiotic resistance. Nat Rev Microbiol 4: 556-562.
49. Lewis, K. (2008) Multidrug tolerance of biofilms and persister cells. Curr Top Microbiol Immunol 322: 107-131.
50. Lewis, K. (2010) Persister cells. Annu Rev Microbiol 64: 357-372.
51. Liñares, J., Ardanuy, C., Pallares, R., and Fenoll, A. (2010) Changes in antimicrobial resistance, serotypes and genotypes in Streptococcus pneumoniae over a 30-year period. Clin Microbiol Infect 16: 402-410.
52. Liu, H.H., and Tomasz, A. (1985) Penicillin tolerance in multiply drug-resistant natural isolates of Streptococcus pneumoniae. J Infect Dis 152: 365-372.
53. Lopez, R., Ronda-Lain, C., Tapia, A., Waks, S.B., and Tomasz, A. (1976) Suppression of the lytic and bactericidal effects of cell wall-inhibitory antibiotics. Antimicrob Agents Chemother 10: 697-706.
54. López, R., and García, E. (2004) Recent trends on the molecular biology of pneumococcal capsules, lytic enzymes, and bacteriophage. FEMS Microbiol Rev 28: 553-580.
55. López, R., Ronda, C., and García, E. (1990) Autolysins are direct involved in the bactericidal effect caused by penicillin in wild type and in tolerant pneumococci. FEMS Microbiol Lett 66: 317-322.
56. McCullers, J.A., English, B.K., and Novak, R. (2000) Isolation and characterization of vancomycin-tolerant Streptococcus pneumoniae from the cerebrospinal fluid of a patient who developed recrudescent meningitis. J Infect Dis 181: 369-373.
57. McDonald, M., Miles, H., Hart, D., and Sonenberg, N. (1980) Penicillin tolerance in Streptococcus faecalis. Lancet 316: 321.
58. Mascher, T., Heintz, M., Zähner, D., Merai, M., and Hakenbeck, R. (2006) The CiaRH system of Streptococcus pneumoniae prevents lysis during stress induced by treatment with cell wall inhibitors and by mutations in pbp2x involved in β-lactam resistance. J Bacteriol 188: 1959-1968.
59. May, J., Shannon, K., King, A., and French, G. (1998) Glycopeptide tolerance in Staphylococcus aureus. J Antimicrob Chemother 42: 189-197.
60. Mlynarcyk, A., Mlynarczyk, B., Kmera-Muszynska, M., Majewski, S., and Mlynarczyk, G. (2009) Mechanisms of the resistance and tolerance to beta-lactam and glycopeptide antibiotics in pathogenic gram-positive cocci. Mini Rev Med Chem 9: 1527-1537.
61. Moscoso, M., Domenech, M., and García, E. (2010) Vancomycin tolerance in clinical and laboratory Streptococcus pneumoniae isolates depends on reduced enzyme activity of the major LytA autolysin or cooperation between CiaH histidine kinase and capsular polysaccharide. Mol Microbiol 77: 1052-1064.
62. Nelson, J.L., Rice, K.C., Slater, S.R., Fox, P.M., Archer, G.L., Bayles, K.W., etal. (2007) Vancomycin-Intermediate Staphylococcus aureus strains have impaired acetate catabolism: implications for polysaccharide intercellular adhesin synthesis and autolysis. Antimicrob Agents Chemother 51: 616-622.
63. Nieto, C., Sadowy, E., Campa, A.G., Hryniewicz, W., and Espinosa, M. (2010) The relBE2Spn toxin-antitoxin system of Streptococcus pneumoniae: role in antibiotic tolerance and functional conservation in clinical isolates. PLoS ONE 5: e11289.
64. Novak, R., Henriques, B., Charpentier, E., Normark, S., and Tuomanen, E. (1999) Emergence of vancomycin tolerance in Streptococcus pneumoniae. Nature 399: 590-593.
65. Novak, R., Charpentier, E., Braun, J.S., and Tuomanen, E. (2000) Signal transduction by a death signal peptide: uncovering the mechanism of bacterial killing by penicillin. Mol Cell 5: 49-57.
66. Perry, J.D., Jones, A.L., and Gould, F.K. (1999) Glycopeptide tolerance in bacteria causing endocarditis. J Antimicrob Chemother 44: 121-124.
67. Potrykus, K., and Cashel, M. (2008) (p)ppGpp: Still Magical? Annu Rev Microbiol 62: 35-51.
68. Pratten, J., and Ready, D. (2010) Use of biofilm model systems to study antimicrobial susceptibility. Methods Mol Biol 642: 203-215.
69. Ramos-Montañez, S., Kazmierczak, K.M., Hentchel, K.L., and Winkler, M.E. (2010) Instability of ackA (acetate kinase) mutations and their effects on acetyl phosphate and ATP amounts in Streptococcus pneumoniae D39. J Bacteriol 192: 6390-6400.
70. Rice, K.C., and Bayles, K.W. (2008) Molecular control of bacterial death and lysis. Microbiol Mol Biol Rev 72: 85-109.
71. Rice, K.C., Nelson, J.B., Patton, T.G., Yang, S.-J., and Bayles, K.W. (2005) Acetic acid induces expression of the Staphylococcus aureus cidABC and lrgAB murein hydrolase regulator operons. J Bacteriol 187: 813-821.
72. Robertson, G.T., Zhao, J., Desai, B.V., Coleman, W.H., Nicas, T.I., Gilmour, R., etal. (2002) Vancomycin tolerance induced by erythromycin but not by loss of vncRS, vex3, or pep27 function in Streptococcus pneumoniae. J Bacteriol 184: 6987-7000.
73. Rodriguez, C.A., Atkinson, R., Bitar, W., Whitney, C.G., Edwards, K.M., Mitchell, L., etal. (2004) Tolerance to vancomycin in pneumococci: detection with a molecular marker and assessment of clinical impact. J Infect Dis 190: 1481-1487.
74. Ronda, C., García, J.L., García, E., Sánchez-Puelles, J.M., and López, R. (1987) Biological role of the pneumococcal amidase. Cloning of the lytA gene in Streptococcus pneumoniae. Eur J Biochem 164: 621-624.
75. Sabath, L.D., Laverdiere, M., Wheeler, N., Blazevic, D., and Wilkinson, B.J. (1977) A new type of penicillin resistance of Staphylococcus aureus. Lancet 309: 443-447.
76. Sader, H.S., Jones, R.N., Rossi, K.L., and Rybak, M.J. (2009) Occurrence of vancomycin-tolerant and heterogeneous vancomycin-intermediate strains (hVISA) among Staphylococcus aureus causing bloodstream infections in nine USA hospitals. J Antimicrob Chemother 64: 1024-1028.
77. Sakoulas, G., Eliopoulos, G.M., Fowler, V.G., Jr, Moellering, R.C., Jr, Novick, R.P., Lucindo, N., etal. (2005) Reduced susceptibility of Staphylococcus aureus to vancomycin and platelet microbicidal protein correlates with defective autolysis and loss of accessory gene regulator (agr) function. Antimicrob Agents Chemother 49: 2687-2692.
78. Sakoulas, G., Gold, H.S., Cohen, R.A., Venkataraman, L., Moellering, R.C., and Eliopoulos, G.M. (2006) Effects of prolonged vancomycin administration on methicillin-resistant Staphylococcus aureus (MRSA) in a patient with recurrent bacteraemia. J Antimicrob Chemother 57: 699-704.
79. Sandoe, J.A.T., Wysome, J., West, A.P., Heritage, J., and Wilcox, M.H. (2006) Measurement of ampicillin, vancomycin, linezolid and gentamicin activity against enterococcal biofilms. J Antimicrob Chemother 57: 767-770.
80. Saribas, S., and Bagdatli, Y. (2004) Vancomycin tolerance in enterococci. Chemotherapy 50: 250-254.
81. Shao, Y., Harrison, E.M., Bi, D., Tai, C., He, X., Ou, H.-Y., etal. (2011) TADB: a web-based resource for Type 2 toxin-antitoxin loci in bacteria and archaea. Nucleic Acids Res 39: D606-D611.
82. Sherris, J.C. (1986) Problems in in vitro determination of antibiotic tolerance in clinical isolates. Antimicrob Agents Chemother 30: 633-637.
83. Sieradzki, K., and Tomasz, A. (2006) Inhibition of the autolytic system by vancomycin causes mimicry of vancomycin-intermediate Staphylococcus aureus-type resistance, cell concentration dependence of the MIC, and antibiotic tolerance in vancomycin-susceptible S. aureus. Antimicrob Agents Chemother 50: 527-533.
84. Singh, R., Ray, P., Das, A., and Sharma, M. (2009) Role of persisters and small-colony variants in antibiotic resistance of planktonic and biofilm-associated Staphylococcus aureus: an in vitro study. J Med Microbiol 58: 1067-1073.
85. Struelens, M.J., and Monnet, D.L. (2010) Prevention of methicillin-resistant Staphylococcus aureus infection: is Europe winning the fight? Infect Control Hosp Epidemiol 31: S42-S44.
86. Sung, H., Shin, H.B., Kim, M.-N., Lee, K., Kim, E.-C., Song, W., etal. (2006) Vancomycin-tolerant Streptococcus pneumoniae in Korea. J Clin Microbiol 44: 3524-3528.
87. Tomasz, A., Albino, A., and Zanati, E. (1970) Multiple antibiotic resistance in a bacterium with suppressed autolytic system. Nature 227: 138-140.
88. Traczewski, M.M., Katz, B.D., Steenergen, J.N., and Brown, S.D. (2009) Inhibitory and bactericidal activities of daptomycin, vancomycin, and teicoplanin against methicillin-resistant Staphylococcus aureus isolates collected from 1985 to 2007. Antimicrob Agents Chemother 53: 1735-1738.
89. Tuomanen, E., Durack, D.T., and Tomasz, A. (1986) Antibiotic tolerance among clinical isolates of bacteria. Antimicrob Agents Chemother 30: 521-527.
90. Vaudaux, P., Huggler, E., Bernard, L., Ferry, T., Renzoni, A., and Lew, D.P. (2010) Underestimation of vancomycin and teicoplanin MICs by broth microdilution leads to underdetection of glycopeptide-intermediate isolates of Staphylococcus aureus. Antimicrob Agents Chemother 54: 3861-3870.
91. Voorn, G., Thompson, J., Goessens, W., Schmal-Bauer, W., Broeders, P., and Michel, M. (1994) In vitro development and stability of tolerance to cloxacillin and vancomycin inStaphylococcus aureus. Eur J Clin Microb Infect Dis 13: 741-746.
92. Weigel, L.M., Clewell, D.B., Gill, S.R., Clark, N.C., McDougal, L.K., Flannagan, S.E., etal. (2003) Genetic analysis of a high-level vancomycin-resistant isolate of Staphylococcus aureus. Science 302: 1569-1571.
93. Wolfe, A.J. (2010) Physiologically relevant small phosphodonors link metabolism to signal transduction. Curr Opin Microbiol 13: 204-209.
94. Wolz, C., Geiger, T., and Goerke, C. (2010) The synthesis and function of the alarmone (p)ppGpp in firmicutes. Int J Med Microbiol 300: 142-147.
95. Xu, X., Lin, D., Yan, G., Ye, X., Wu, S., Guo, Y., etal. (2010) vanM, a new glycopeptide resistance gene cluster found in Enterococcus faecium. Antimicrob Agents Chemother 54: 4643-4647.
96. Yoon, Y.K., Kim, J.Y., Park, D.W., Sohn, J.W., and Kim, M.J. (2010) Predictors of persistent methicillin-resistant Staphylococcus aureus bacteraemia in patients treated with vancomycin. J Antimicrob Chemother 65: 1015-1018.
97. Zaoutis, T., Schneider, B., Steele Moore, L., and Klein, J.D. (1999) Antibiotic susceptibilities of group C and Group G streptococci isolated from patients with invasive infections: evidence of vancomycin tolerance among group G serotypes. J Clin Microbiol 37: 3380-3383.
98. Zapun, A., Contreras-Martel, C., and Vernet, T. (2008) Penicillin-binding proteins and β-lactam resistance. FEMS Microbiol Rev 32: 361-385.
99. Zhanel, G.G., Calic, D., Schweizer, F., Zelenitsky, S., Adam, H., Lagacé-Wiens, P.R.S., etal. (2010) New lipoglycopeptides. A comparative review of dalbavancin, oritavancin and telavancin. Drugs 70: 859-886.
100. Zhu, T., Lou, Q., Wu, Y., Hu, J., Yu, F., and Qu, D. (2010) Impact of the Staphylococcus epidermidis LytSR two-component regulatory system on murein hydrolase activity, pyruvate utilization and global transcriptional profile. BMC Microbiol 10: 287.