Minimal attachment killing (MAK): A versatile method for susceptibility testing of attached biofilm-positive and -negative Staphylococcus epidermidis

Medical Microbiology and Immunology

Volumn 191, Issue 2, 2002, Pages 107-114

  Knobloch, Johannes K M ^a   Von Osten, Heimke ^a   Horstkotte, Matthias A ^a   Rohde, Holger ^a   Mack, Dietrich ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

Antibiotics; Biofilm; Persister; Resistance; Staphylococcus

Indexed keywords

GENTAMICIN; OXACILLIN; PENICILLIN G; VANCOMYCIN;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL INFECTION; BACTERIAL STRAIN; BACTERIUM ADHERENCE; BACTERIUM ISOLATE; BACTERIUM MUTANT; BIOFILM; CONTROLLED STUDY; FOREIGN BODY; HOSPITAL INFECTION; MINIMAL ATTACHMENT KILLING; NONHUMAN; PHENOTYPE; PREDICTION; PRIORITY JOURNAL; STAPHYLOCOCCUS EPIDERMIDIS; TREATMENT FAILURE; TREATMENT OUTCOME;

ANTI-BACTERIAL AGENTS; BACTERIAL ADHESION; BIOFILMS; DRUG RESISTANCE, MICROBIAL; MICROBIAL SENSITIVITY TESTS; MODELS, BIOLOGICAL; STAPHYLOCOCCUS EPIDERMIDIS;

EID: 0036400721     PISSN: 03008584     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00430-002-0125-2     Document Type: Article

References (52)

1. Amorena B, Gracia E, Monzon M, Leiva J, Oteiza C, Perez M, Alabart JL, Hernandez-Yago J (1999) Antibiotic susceptibility assay for Staphylococcus aureus in biofilms developed in vitro. J Antimicrob Chemother 44:43-55
2. Anwar H, Strap JL, Costerton JW (1992) Eradication of biofilm cells of Staphylococcus aureus with tobramycin and cephalexin. Can J Microbiol 38:618-625
3. Arciola CR, Baldassarri L, Montanaro L (2001) Presence of icaA and icaD genes and slime production in a collection of staphylococcal strains from catheter-associated infections. J Clin Microbiol 39:2151-2156
4. Baddour LM, Smalley DL, Hill MM, Christensen GD (1988) Proposed virulence factors among coagulase-negative staphylococci isolated from two healthy populations. Can J Microbiol 34:901-905
5. Berthaud N, Desnottes JE (1997) In vitro bactericidal activity of quinupristin/dalfopristin against adherent Staphylococcus aureus. J Antimicrob Chemother 39 Suppl A:99-102
6. Cagni A, Chuard C, Vaudaux PE, Schrenzel J, Lew DP (1995) Comparison of sparfloxacin, temafloxacin, and ciprofloxacin for prophylaxis and treatment of experimental foreign-body infection by methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 39:1655-1660
7. Ceri H, Olson ME, Stremick C, Read RR, Morek D, Buret A (1999) The Calgary Biofilm Device: new technology for rapid determination of antibiotic susceptibilities of bacterial biofilms. J Clin Microbiol 37:1771-1776
8. Ceri H, Olson M, Morck D, Storey D, Read R, Buret A, Olson B (2001) The MBEC assay system: multiple equivalent biofilms for antibiotic and biocide susceptibility testing. Methods Enzymol 337:377-385
9. Christensen GD, Simpson WA, Bisno AL, Beachey EH (1982) Adherence of slime-producing strains of Staphylococcus epidermidis to smooth surfaces. Infect Immun 37:318-326
10. Christensen GD, Baldassari L, Simpson WA (1994) Colonisation of medical devices by coagulase-negative staphylococci. In: Waldvogel FA, Bisno AL (eds) Infection associated with indwelling medical divices, pp 45-78
11. Cramton SE, Ulrich M, Götz F, Döring G (2001) Anaerobic conditions induce expression of polysaccharide intercellular adhesin in Staphylococcus aureus and Staphylococcus epidermidis. Infect Immun 69:4079-4085
12. Duguid IG, Evans E, Brown MR, Gilbert P (1992) Effect of biofilm culture upon the susceptibility of Staphylococcus epidermidis to tobramycin. J Antimicrob Chemother 30:803-810
13. Espersen F, Frimodt-Moller N, Corneliussen L, Thamdrup RV, Skinhoj P (1993) Experimental foreign body infection in mice. J Antimicrob Chemother 31 Suppl D:103-111
14. Francois P, Vaudaux P, Lew PD (1998) Role of plasma and extracellular matrix proteins in the physiopathology of foreign body infections. Ann Vasc Surg 12:34-40
15. Galdbart JO, Allignet J, Tung HS, Ryden C, EI Solh N (2000) Screening for Staphylococcus epidermidis markers discriminating between skin-flora strains and those responsible for infections of joint prostheses. J Infect Dis 182:351-355
16. Götz F, Peters G (2000) Colonization of medical devices by coagulase-negative staphylococci. In: Waldvogel FA, Bisno AL, (eds) Infections associated with indwelling medical devices. ASM Press, Washington DC, pp 55-88
17. Hamilton-Miller JM, Shah S (1997) Activity of quinupristin/dalfopristin against Staphylococcus epidermidis in biofilms: a comparison with ciprofloxacin. J Antimicrob Chemother 39 Suppl A:103-108
18. Heilmann C, Schweitzer O, Gerke C, Vanittanakom N, Mack D, Götz F (1996) Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis. Mol Microblol 20:1083-1091
19. Jorgensen JH, Turnidge JD, Washington JA (1999) Antibacterial susceptibility tests: dilution and disk diffusion methods. In: Murray PR (ed) Manual of clinical microbiology. ASM Press, Washington DC, pp 1526-1543
20. Knobloch JK, Bartscht K, Sabottke A, Rohde H, Feucht HH, Mack D (2001) Biofilm formation by Staphylococcus epidermidis depends on functional RsbU, an activator of the sigB operon: differential activation mechanisms due to ethanol and salt stress. J Bacteriol 183:2624-2633
21. Knobloch JK, Horstkotte MA, Rohde H, Kaulfers PM, Mack D (2002) Alcoholic ingredients in skin disinfectants increase biofilm expression of Staphylococcus epidermidis. J Antimicrob Chemother 49:683-687
22. König C, Schwank S, Blaser S (2001) Factors compromising antibiotic activity against biofilms of Staphylococcus epidermidis. Eur J Clin Microbiol Infect Dis 20:20-26
23. Lewis K (2000) Programmed death in bacteria. Microbiol Mol Biol Rev 64:503-514
24. Lucet JC, Herrmann M, Rohner P, Auckenthaler R, Waldvogel FA, Lew DP (1990) Treatment of experimental foreign body infection caused by methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 34:2312-2317
25. Mack D, Siemssen N, Laufs R (1992) Parallel induction by glucose of adherence and a polysaccharide antigen specific for plastic-adherent Staphylococcus epidermidis: evidence for functional relation to intercellular adhesion. Infect Immun 60:2048-2057
26. Mack D, Fischer W, Krokotsch A, Leopold K, Hartmann R, Egge H, Laufs R (1996) The intercellular adhesin involved in biofilm accumulation of Staphylococcus epidermidis is a linear beta-1,6-linked glucosaminoglycan: purification and structural analysis. J Bacteriol 178:175-183
27. Mack D, Haeder M, Siemssen N, Laufs R (1996) Association of biofilm production of coagulase-negative staphylococci with expression of a specific polysaccharide intercellular adhesin. J Infect Dis 174:881-884
28. Mack D, Riedewald J, Rohde H, Magnus T, Feucht HH, Elsner HA, Laufs R, Rupp ME (1999) Essential functional role of the polysaccharide intercellular adhesin of Staphylococcus epidermidis in hemagglutination. Infect Immun 67:1004-1008
29. Mack D, Bartscht K, Fischer C, Rohde H, Grahl C de, Dobinsky S, Horstkotte MA, Kiel K, Knobloch JK (2001) Genetic and biochemical analysis of Staphylococcus epidermidis biofilm acciumulation. Methods Enzymol 336:215-239
30. Mack D, Sabottke A, Dobinsky S, Rohde H, Horstkotte MA, Knobloch JK (2002) Differential expression of methicillin resistance by different biofilm-negative Staphylococcus epidermidis transposon mutant classes. Antimicrob Agents Chemother 46:178-183
31. Marrie TJ, Nelligan J, Costerton JW (1982) A scanning and transmission electron microscopic study of an infected endocardial pacemaker lead. Circulation 66:1139-1341
32. Nedelmann M, Sabottke A, Laufs R, Mack D (1998) Generalized transduction for genetic linkage analysis and transfer of transposon insertions in different Staphylococcus epidermidis strains. Zentralbl Bakteriol 287:85-92
33. Peters G, Locci R, Pulverer G (1981) Microbial colonization of prosthetic devices. II. Scanning electron microscopy of naturally infected intravenous catheters. Zentralbl Bakteriol Mikrobiol Hyg [B] 173:293-299
34. Rachid S, Cho S, Ohlsen K, Hacker J, Ziebuhr W (2000) Induction of Staphylococcus epidermidis biofilm formation by environmental factors: the possible involvement of the alternative transcription factor sigB. Adv Exp Med Biol 485:159-166
35. Rohde H, Knobloch JK, Horstkotte MA, Mack D (2001) Correlation of biofilm expression types of Staphylococcus epidermidis with polysaccharide intercellular adhesin synthesis: evidence for involvement of icaADBC genotype-independent factors. Med Microbiol Immunol (Berl) 190:105-112
36. Rupp ME, Ulphani JS, Fey PD, Bartscht K, Mack D (1999) Characterization of the importance of polysaccharide intercellular adhesin/hemagglutinin of Staphylococcus epidermidis in the pathogenesis of biomaterial-based infection in a mouse foreign body infection model. Infect Immun 67:2627-2632
37. Rupp ME, Ulphani JS, Fey PD, Mack D (1999) Characterization of Staphylococcus epidermidis polysaccharide intercellular adhesin/hemagglutinin in the pathogenesis of intravascular catheter-associated infection in a rat model. Infect Immun 67:2656-2659
38. Rupp ME, Fey PD, Heilmann C, Götz F (2001) Characterization of the importance of Staphylococcus epidermidis autolysin and polysaccharide intercellular adhesin in the pathogenesis of intravascular catheter-associated infection in a rat model. J Infect Dis 183:1038-1042
39. Schaad HJ, Chuard C, Vaudaux P, Rohner P, Waldvogel FA, Lew DP (1994) Comparative efficacies of imipenem, oxacillin and vancomycin for therapy of chronic foreign body infection due to methicillin-susceptible and -resistant Staphylococcus aureus. J Antimicrob Chemother 33:1191-1200
40. Schaad HJ, Chuard C, Vaudaux P, Waldvogel FA, Lew DP (1994) Teicoplanin alone or combined with rifampin compared with vancomycin for prophylaxis and treatment of experimental foreign body infection by methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 38:1703-1710
41. Schierholz JM, Beuth J, König D, Nürnberger A, Pulverer G (1999) Antimicrobial substances and effects on sessile bacteria. Zentralbl Bakteriol 289:165-177
42. Schwank S, Rajacic Z, Zimmerli W, Blaser J (1998) Impact of bacterial biofilm formation on in vitro and in vivo activities of antibiotics. Antimicrob Agents Chemother 42:895-898
43. Spoering AL, Lewis K (2001) Biofilms and planktonic cells of Pseudomonas aeruginosa have similar resistance to killing by antimicrobials. J Bacteriol 183:6746-6751
44. Stein A, Drancourt M, Raoult D (2000) Ambulatory management of infected orthopedic implants. In: Waldvogel FA, Bisno AL (eds) Infections associated with indwelling medical devices. ASM Press, Washington DC, pp 211-230
45. Vaudaux P, Yasuda H, Velazco MI, Huggler E, Ratti I, Waldvogel FA, Lew DP, Proctor RA (1990) Role of host and bacterial factors in modulating staphylococcal adhesion to implanted polymer surfaces. J Biomater Appl 5:134-153
46. Vaudaux PE, Zulian G, Huggler E, Waldvogel FA (1985) Attachment of Staphylococcus aureus to polymethylmethacrylate increases its resistance to phagocytosis in foreign body infection. Infect Immun 50:472-477
47. Vaudaux PE, Francois P, Proctor RA, McDevitt D, Foster TJ, Albrecht RM, Lew DP, Wabers H, Cooper SL (1995) Use of adhesion-defective mutants of Staphylococcus aureus to define the role of specific plasma proteins in promoting bacterial adhesion to canine arteriovenous shunts. Infect Immun 63:585-590
48. Yasuda H, Ajiki Y, Koga T, Yokota T (1994) Interaction between clarithromycin and biofilms formed by Staphylococcus epidermidis. Antimicrob Agents Chemother 38:138-141
49. Zelver N, Hamilton M, Pitts B, Goeres D, Walker D, Sturman P, Heersink J (1999) Measuring antimicrobial effects on biofilm bacteria: from laboratory to field. Methods Enzymol 30:608-628
50. Ziebuhr W, Heilmann C, Gotz F, Meyer P, Wilms K, Straube E, Hacker J (1997) Detection of the intercellular adhesion gene cluster (ica) and phase variation in Staphylococcus epidermidis blood culture strains and mucosal isolates. Infect Immun 65:890-896
51. Zimmerli W, Lew PD, Waldvogel FA (1984) Pathogenesis of foreign body infection. Evidence for a local granulocyte defect. J Clin Invest 73:1191-1200
52. Zimmerli W, Widmer AF, Blatter M, Frei R, Ochsner PE (1998) Role of rifampin for treatment of orthopedic implant-related staphylococcal infections: a randomized controlled trial. Foreign-Body Infection (FBI) Study Group. JAMA 279:1537-1541