Antibiotic susceptibility assay for Staphylococcus aureus in biofilms developed in vitro

Journal of Antimicrobial Chemotherapy

Volumn 44, Issue 1, 1999, Pages 43-55

  Amorena, Beatriz ^a,d   Gracia, Elena ^a,e   Monzón, Marta ^a   Leiva, José ^b   Oteiza, Concepción ^b   Pérez, Marta ^a   Alabart, José Luis ^a   Hernández Yago, José ^c  

^a CSIC   (Spain)

^b UNIVERSITY CLINIC OF NAVARRA   (Spain)

^c Inst of Cytological Investigations   (Spain)

^d Centro de Investigación y Tecnología Agroalimentaria de Aragón   (Spain)

^e Centro Salud San Mateo de Gállego   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CEFAZOLIN; CEFUROXIME; CIPROFLOXACIN; ERYTHROMYCIN; FOSFOMYCIN; GENTAMICIN; NOVOBIOCIN; PENICILLIN G; RIFAMPICIN; TOBRAMYCIN; VANCOMYCIN;

ANTIBIOTIC SENSITIVITY; ARTICLE; BIOFILM; BIOLUMINESCENCE; CELL DENSITY; CELL VIABILITY; CELLULAR DISTRIBUTION; COMPARATIVE STUDY; CONTROLLED STUDY; CULTURE MEDIUM; IN VITRO STUDY; MILK; STAPHYLOCOCCUS AUREUS; TRANSMISSION ELECTRON MICROSCOPY;

ADENOSINE TRIPHOSPHATE; ANTI-BACTERIAL AGENTS; BIOFILMS; CULTURE MEDIA; HUMANS; LUMINESCENT MEASUREMENTS; MICROBIAL SENSITIVITY TESTS; MICROSCOPY, ELECTRON; STAPHYLOCOCCUS AUREUS;

EID: 0032856709     PISSN: 03057453     EISSN: None     Source Type: Journal    
DOI: 10.1093/jac/44.1.43     Document Type: Article

References (72)

1. Costerton, J. W., Cheng, K. J., Geesey, G. G., Ladd, T. I., Nickel, J. C., Dasgupta, M. et al. (1987). Bacterial biofilms in nature and diseases. Annual Review of Microbiology 41, 435-64.
2. Gristina, A. G., Hobgood, C. D., Webb, L. X. & Myrvik, Q. N. (1987). Adhesive colonization of biomaterials and antibiotic resistance. Biomaterials 8, 423-6.
3. National Committee for Clinical Laboratory Standards. (1990). Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically-Second Edition: Approved Standard M7-A2. NCCLS, Villanova, PA.
4. Chuard, C., Lucet, J., Rohner, P., Herrmann, M., Auckenthaler, R., Waldvogel, F. et al. (1991). Resistance of Staphylococcus aureus recovered from infected foreign body in vivo to killing by antimicrobials. Journal of Infectious Diseases 163, 1369-73.
5. Kaatz, G., Seo, S., Dorman, N. & Lerner, S. (1990). Emergence of teicoplanin resistance during therapy of Staphylococcus aureus endocarditis. Journal of Infectious Diseases 162, 103-8.
6. Anwar, H., Van Biesen, T., Dasgupta, M., Lam, K. & Costerton, J.W. (1989). Interaction of biofilm bacteria with antibiotics in a novel in-vitro chemostat system. Antimicrobial Agents and Chemotherapy 33, 1824-6.
7. Christensen, G. D., Simpson, W. A., Younger, J. J., Baddour, L. M., Barret, F. F., Melton, D. M. et al. (1985). Adherence of coagulase-negative staphylococci to plastic tissue culture plates: a quantitative model for the adherence of staphylococci to medical device. Journal of Clinical Microbiology 22, 996-1006.
8. Chuard, C., Vaudaux, P., Waldvogel, F. A. & Lew., D. P. (1993). Susceptibility of Staphylococcus aureus growing on fibronectin-coated surfaces to bactericidal antibiotics. Antimicrobial Agents and Chemotherapy 37, 625-32.
9. Domingue, G., Ellis, B., Dasgupta, M. & Costerton, J. W. (1994). Testing antimicrobial susceptibilities of adherent bacteria by a method that incorporates guidelines of the National Committee for Clinical Laboratory Standards. Journal of Clinical Microbiology 32, 2564-8.
10. Marrie, T. J., Nelligan, J. & Costerton, J. W. (1982). A scanning and transmission electron microscopic study of an infected endocardial pacemaker lead. Circulation 66, 1339-41.
11. Wirtanen, G. & Sandholm, T. M. (1992). Effect of the growth phase of foodborne biofilms on their resistance to a chlorine sanitizer Part II. Lebensmittel-Wissenschaft + Technologie 25, 50-4.
12. Ordóñez, J. V. & Wehman, N. M. (1993). Rapid flow cytometric antibiotic susceptibility assay for Staphylococcus aureus. Cytometry 14, 811-18.
13. Hussain, M., Collins, C., Hastings, G. M. & White, P. J. (1992). Radiochemical assay to measure the biofilm produced by coagulase-negative staphylococci on solid surfaces and its use to quantify the effects of various antibacterial compounds on the formation of the biofilm. Journal of Medical Microbiology 37, 62-69.
14. de Rautlin de la Roy, Y., Messedi, N., Grollier, G. & Grignon, B. (1991). Kinetics of bactericidal activity of antibiotics measured by luciferin-luciferase assay. Journal of Bioluminescence and Chemiluminescence 6, 193-201.
15. Stanley, B. J. & McCarthy, B. J. (1989). Reagents and instruments for assays using ATP and luminescence: present needs and future possibilities in rapid microbiology. In Rapid Methods in Microbiology. ATP Luminescence (Stanley, P. E., McCarthy, B. J. & Smither, R., Eds), pp. 73-80. Society for Applied Bacteriology. Technical Series. No. 26. Blackwell, Boston, MA.
16. Wheat, P. F., Hastings, J. G. & Spencer, R. C. (1988). Rapid antibiotic susceptibility tests on Enterobacteriaceae by ATP bioluminescence. Journal of Medical Microbiology 25, 95-9.
17. Vasavada, P. (1993). Rapid methods and automation in dairy microbiology. Symposium: evaluation of milk and dairy products. Journal of Dairy Science 76, 3101-13.
18. Cooksey, R. C., Morlock, G. P., Beggs, M. & Crawford, J. T. (1995). Bioluminescence method to evaluate antimicrobial agents against Mycobacterium avium. Antimicrobial Agents and Chemotherapy 39, 754-6.
19. Stemke, W. G. & Robertson, J. (1990). The growth response of Mycoplasma hyopneumoniae and Mycoplasma flocculare based upon ATP-dependent luminometry. Veterinary Microbiology 24, 135-42.
20. Baselga, R., Albizu, I., De la Cruz, M., Del Cacho, E., Barberán, M. & Amorena, B. (1993). Phase variation of slime production in Staphylococcus aureus: implications in colonization and virulence. Infection and Immunity 61, 4857-62.
21. Baselga, R., Albizu, I., Aguilar, B., Iturralde, M. & Amorena, B. (1992). Hydrophobicity of ruminant mastitis Staphylococcus aureus in relation to bacterial aging and slime production. Current Microbiology 25, 173-9.
22. Gracia, E., Fernández, A., Conchello, P., Laclériga, A., Paniagua, L., Seral, F. et al. (1997). Adherence of Staphylococcus aureus slime-producing strain variants to biomaterials used in orthopaedic surgery. International Orthopaedics 21, 46-51.
23. Freeman, D. J., Falkiner, F. R. & Keane, C. T. (1989). New method for detecting slime production by coagulase negative staphylococci. Journal of Clinical Pathology 42, 872-4.
24. Popovic, T., Bopp, Ch. A., Olsvik, O. & Kiehlbaugh, J. A. (1993). Ribotyping in molecular epidemiology. In Diagnostic Molecular Microbiology. Principles and Applications (Persing, D. H., Smith, T. F., Tennover, F. C. & White, T. J., Eds), pp. 573-63. American Society for Microbiology, Washington, DC.
25. Anwar, H., Strap, J. L. & Costerton, J. W. (1992). Eradication of biofilm cells of Staphylococcus aureus with tobramycin and cephalexin. Canadian Journal of Microbiology 38, 618-25.
26. Gracia, E. (1997). Test de sensibilidad a antibióticos para Staphylococcus aureus formadores de biofilms. Doctoral thesis, University of Zaragoza, Zaragoza, Spain.
27. Statistical Analysis Systems Institute, Inc. (1989). SAS/STAT User's Guide, Version 6, Fourth Edition, Volume 1. SAS Institute, Inc., Cary, NC.
28. Anwar, H., Strap, J. L. & Costerton, J. W. (1992). Establishment of aging biofilms: possible mechanism of bacterial resistance to antimicrobial therapy. Antimicrobial Agents and Chemotherapy 36, 1347-51.
29. Brown, M. R., Allison, D. G. & Gilbert, P. (1988). Resistance of bacterial biofilms to antibiotics: a growth-rate related effect? Journal of Antimicrobial Chemotherapy 22, 777-83.
30. Dall, L. & Herndon, B. (1989). Quantitative assay of glycocalyx produced by viridians group streptococci that cause endocarditis. Journal of Clinical Microbiology 279, 2039-41.
31. Fraber, B. F., Kaplan, M. H. & Clogston, A. (1990). Staphylococcus epidermidis extracted slime inhibits the antimicrobial action of glycopeptide antibiotics. Journal of Infectious Diseases 161, 37-40.
32. Brandt, C. M., Rouse, M. S., Tallan, B. M., Laue, N. W., Wilson, W. R. & Steckelberg, J. M. (1995). Effective treatment or cephalosporin-rifampicin combinations against cryptic methicillin-resistant β-lactamase-producing coagulase-negative staphylococcal experimental endocarditis. Antimicrobial Agents and Chemotherapy 39, 1815-19.
33. Dunne, W. M., Mason, E. O. & Kaplan, S. L. (1993). Diffusion of rifampicin and vancomycin through a Staphylococcus epidermidis biofilm. Antimicrobial Agents and Chemotherapy 37, 2522-6.
34. Prosser, B. L., Taylor, D., Dix, B. A. & Cleeland, R. (1987). Method of evaluating effects of antibiotics on bacterial biofilm. Antimicrobial Agents and Chemotherapy 31, 1502-6.
35. Vorachit, M., Lam, K., Jayanetra, P. & Costerton, J. W. (1993). Resistance of Pseudomonas pseudomallei growing as a biofilm on silastic discs to ceftazimide and co-trimoxazole. Antimicrobial Agents and Chemotherapy 37, 2000-2.
36. Nickel, J. C., Ruseska, I., Wright, J. B. & Costerton, J. W. (1985). Tobramycin resistance of Pseudomonas aeruginosa cells growing as a biofilm on urinary catheter material. Antimicrobial Agents and Chemotherapy 27, 619-24.
37. Barth, E., Myrvik, Q. M., Wagner, W. & Gristina, A. G. (1989). In-vitro and in-vivo colonization of Staphylococcus aureus and Staphylococcus epidermidis on orthopaedic implant materials. Biomaterials 10, 325-8.
38. Pore, R. S. (1994). Antibiotic susceptibility testing by flow cytometry. Journal of Antimicrobial Chemotherapy 34, 613-27.
39. Berthaud, N., Huet, Y., Diallo, N. & Desnotes, J.-F. (1997). Antistaphylococcal activities of quinupristin/dalfopristin in vitro across platelet-fibrin matrices and in experimental endocarditis. Journal of Antimicrobial Chemotherapy 39, Suppl. A, 93-8.
40. Hamilton-Miller, J. M. T. & Shah, S. (1997). Activity of quinupristin/dalfopristin against Staphylococcus epidermidis in biofilms: a comparison with ciprofloxacin. Journal of Antimicrobial Chemotherapy 39, Suppl. A, 103-8.
41. Bolourchi, M., Hovareshti, P. & Tabatabayi, A. (1995). Comparison of the effects of local and systemic dry cow therapy for staphylococcal mastitis control. Preventive Veterinary Medicine 25, 63-7.
42. Perdikaris, G. S., Pefanis, A., Giamarellou, H., Nikolopoulos, A., Margaris, E. P., Donta, I. et al. (1997). Successful single-dose teicoplanin prophylaxis against experimental streptococcal, enterococcal, and staphylococcal aortic valve endocarditis. Antimicrobial Agents and Chemotherapy 41, 1916-21.
43. Pérez Fernández, P., Herrera, I., Martínez, P., Gómez-Lus, M. L. & Prieto, J. (1995). Enhancement of the susceptibility of Staphylococcus aureus to phagocytosis after treatment with phosphomycin compared with other antimicrobial agents. Chemotherapy 41, 45-49.
44. Ramírez de Arellano, E., Pascual, A., Martínez-Martínez, L. & Perea, E. J. (1994). Activity of eight antibacterial agents on Staphylococcus epidermidis attached to Teflon catheters. Journal of Medical Microbiology 40, 43-7.
45. Drancourt, M., Stein, A., Argenson, J. N., Roiron, R., Groulier, P. & Raoult, D. (1997). Oral treatment of Staphylococcus spp. infected orthopaedic implants with fusidic acid or ofloxacin in combination with rifampicin. Journal of Antimicrobial Chemotherapy 39, 235-40.
46. Widmer, A. F., Frei, R., Rajacic, Z. & Zimmerli, W. (1990). Correlation between in-vivo and in-vitro efficacy of antimicrobial agents against foreign body infections. Journal of Infectious Diseases 162, 96-102.
47. Gander, S. (1996). Bacterial biofilms: resistance to antimicrobial agents. Journal of Antimicrobial Agents 37, 1047-50.
48. Balows, A., Hausler, W. J., Herrmann, K. L. & Shadomy, H. J. (1991). Manual of Clinical Microbiology. American Society for Microbiology, Washington, DC.
49. Baquero, F. & Cantón, R. (1996). In-vitro activity of sparfloxacin in comparison with currently available antimicrobials against respiratory tract pathogens. Journal of Antimicrobial Chemotherapy 37, Suppl.A, 1-18.
50. Endtz, H. P., Mouton, J. W., Den Hollander, J. G., van den Braak, N. & Verbrugh, H. A. (1997). Comparative in-vitro activities of trovafloxacin (CP-99,219) against 445 Gram-positive isolates from patients with endocarditis and those with other bloodstream infections. Antimicrobial Agents and Chemotherapy 41, 1146-9.
51. 14C]sparfloxacin in experimental Staphylococcus aureus joint prosthesis infection. Antimicrobial Agents and Chemotherapy 40, 2111-16.
52. Kaatz, G. W., Seo, S. M., Aeschlimann, J. R., Houlihan, H. H., Mercier, R.-C. & Rybak, M. J. (1998). Efficacy of trovafloxacin against experimental Staphylococcus aureus endocarditis. Antimicrobial Agents and Chemotherapy 42, 254-6.
53. Maserati, R., Cagni, A. E. & Segú, C. (1996). Sparfloxacin therapy for experimental endocarditis caused by methicillin-resistant Staphylococcus aureus. Chemotherapy 42, 133-9.
54. Pemán, J., Cantón, E., Hernández, M. T. & Gobernado, M. (1994). Intraphagocytic killing of Gram-positive bacteria by ciprofloxacin. Journal of Antimicrobial Chemotherapy 34, 965-74.
55. Sánchez, M. S., Ford, C. W. & Yancey, R. J. (1988). Evaluation of antibiotic effectiveness against Staphylococcus aureus surviving within the bovine mammary grand macrophage. Journal of Antimicrobial Chemotherapy 21, 773-86.
56. Sandholm, M., Kaartinen, L. & Pyorala, S. (1990). Bovine mastitis - why does antibiotic therapy not always work? An overview. Journal of Veterinary Pharmacology and Therapy 13, 248-60.
57. Kang, S. L., Rybak, M. J., McGrath, B. J., Kaatz, G. W. & Seo, S. M. (1994). Pharmacodynamics of levofloxacin, ofloxacin, and ciprofloxacin, alone and in combination with rifampicin, against methicillin-susceptible and resistant Staphylococcus aureus in an invitro infection model. Antimicrobial Agents and Chemotherapy 38, 2702-9.
58. Nieto, M. & Perkins, H. R. (1971). Physicochemical properties of vancomycin and iodovancomycin and their complexes with diacetyl-L-lysyl-D-alanyl-D-alanine. Biochemical Journal 123, 773-87.
59. Daschner, F. D. & Kropec, A. (1995). Glycopeptides in the treatment of staphylococcal infections. European Journal of Clinical Microbiology and Infectious Diseases 14, Suppl. 1, S12-17.
60. Evans, R. & Clifford, J. H. (1987). Effect of vancomycin hydrochloride on Staphylococcus epidermidis biofilm associated with silicone elastomer. Antimicrobial Agents and Chemotherapy 31, 889-94.
61. Darouiche, R. O., Dhir, A., Miller, A. J., Landon, G. C., Raad, I. I. & Musher, D. M. (1994). Vancomycin penetration into biofilm covering infected prostheses and effect on bacteria. Journal of Infectious Diseases 170, 720-3.
62. Houlihan, H. H., Mercier, R. C. & Ryback, M. J. (1997). Pharmacodynamics of vancomycin alone and in combination with gentamicin at various dosing intervals against methicillin-resistant Staphylococcus aureus-infected fibrin-platelet clots in an in-vitro infection model. Antimicrobial Agents and Chemotherapy 41, 2497-501.
63. Schmitz, F.-J. & Jones, M. E. (1997). Antibiotics for treatment of infections caused by MRSA and elimination of MRSA carriage. What are the choices? International Journal of Antimicrobial Agents 9, 1-19.
64. Raymond, J., Vedel, G. & Begeret, M. (1996). In-vitro bactericidal activity of cefpirome in combination with vancomycin against Staphylococcus aureus and coagulase-negative staphylococci. Journal of Antimicrobial Chemotherapy 38, 1067-71.
65. Berthaud, N. & Desnotes, J.-F. (1997). In-vitro bactericidal activity of quinupristin/dalfopristin against adherent Staphylococcus aureus. Journal of Antimicrobial Chemotherapy 39, Suppl. A, 99-102.
66. Tardáguila, J., Gonzalo, C., Marco, J. C. & San Primitivo, F. (1997). Eficacia al parto de 2 métodos de tratamiento antibiótico de secado en el ovino lechero de raza Churra. Informe Técnico Económico Agrícola Suppl. 18, 552-4.
67. Fassel, T. A., Mozdiak, P. E., Sanger, J. R. & Edmiston, C. E. (1997). Paraformaldehyde effect on ruthenium red and lysine preservation and staining of the staphylococcal glycocalyx. Microscopy Research and Technique 36, 422-7.
68. Gristina, A. G., Dobbins, J. J., Giammara, B., Lewis, J. C. & DeVries, W. C. (1988). Biomaterial-centered sepsis and the total artificial heart microbial adhesion vs tissue integration. Journal of the American Medical Association 259, 870-4.
69. Passerini, L., Lam, K., Costerton, J. W. & King, E. G. (1992). Biofilms on indwelling vascular catheters. Critical Care Medicine 20, 665-73.
70. Mayberry-Carson, K. J., Mayberry, W. R., Tober-Meyer, B. K., Costerton, J. W. & Lambe, D. W. (1986). An electron microscopic study on the effect of clindamycin on adherence of Staphylococcus aureus to bone surfaces. Microbiosi 45, 21-32.
71. Gracia, E., Laclériga, A., Monzón, M., Leiva, J., Oteiza, C. & Amorena, B. (1999). Application of a rat osteomyelitis model to compare in vivo and in vitro the antibiotic efficacy against bacteria with high capacity to form biofilms. Journal of Surgical Research 79, 146-53.
72. Bamberger, D., Fields, M. & Herndon, B. (1991). Efficacies of various antimicrobial agents in treatment of Staphylococcus aureus abscess and correlation with in-vitro tests of antimicrobial activity and neutrophil killing. Antimicrobial Agents and Chemotherapy 35, 2335-9.