Influence of surface characteristics of implant materials on MRSA biofilm formation and effects of antimicrobial treatment

IntroductionOne of the main causes of treatment failure in bacterial prosthetic joint infections (PJI) is biofilm formation. The topography of the biofilm may be associated with susceptibility to antimicrobial treatment. The aims of this study were to assess differences in topography of biofilms on...

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Main Authors: Sven C. J. van Dun, Mariëlle Verheul, Bart G. C. W. Pijls, Joffrey van Prehn, Henk Scheper, Federica Galli, Peter H. Nibbering, Mark G. J. de Boer
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-04-01
Series:Frontiers in Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1145210/full
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author Sven C. J. van Dun
Mariëlle Verheul
Bart G. C. W. Pijls
Joffrey van Prehn
Henk Scheper
Federica Galli
Peter H. Nibbering
Mark G. J. de Boer
author_facet Sven C. J. van Dun
Mariëlle Verheul
Bart G. C. W. Pijls
Joffrey van Prehn
Henk Scheper
Federica Galli
Peter H. Nibbering
Mark G. J. de Boer
author_sort Sven C. J. van Dun
collection DOAJ
description IntroductionOne of the main causes of treatment failure in bacterial prosthetic joint infections (PJI) is biofilm formation. The topography of the biofilm may be associated with susceptibility to antimicrobial treatment. The aims of this study were to assess differences in topography of biofilms on different implant materials and the correlation thereof with susceptibility to antimicrobial treatment.MethodsMethicillin-resistant Staphylococcus aureus (MRSA) 7-day mature biofilms were generated on disks made from titanium alloys (Ti-6Al-7Nb and Ti-6Al-4V), synthetic polymer and orthopedic bone cement, commonly used in implant surgery. The surface topography of these implant materials and the biofilms cultured on them was assessed using atomic force microscopy. This provided detailed images, as well as average roughness (Ra) and peak-to-valley roughness (Rt) values in nanometers, of the biofilm and the material surfaces. Bacterial counts within biofilms were assessed microbiologically. Antimicrobial treatment of biofilms was performed by 24-h exposure to the combination of rifampicin and ciprofloxacin in concentrations of 1-, 5- and 10-times the minimal bactericidal concentration (MBC). Finally, treatment-induced differences in bacterial loads and their correlation with biofilm surface parameters were assessed.ResultsThe biofilm surfaces on titanium alloys Ti-6Al-7Nb (Ra = 186 nm) and Ti-6Al-4V (Ra = 270 nm) were less rough than those of biofilms on silicone (Ra = 636 nm). The highest roughness was observed for biofilms on orthopedic bone cement with an Ra of 1,551 nm. Interestingly, the roughness parameters of the titanium alloys themselves were lower than the value for silicone, whereas the surface of the bone cement was the roughest. Treatment with 1- and 5-times the MBC of antibiotics resulted in inter-material differences in colony forming units (CFU) counts, ultimately showing comparable reductions of 2.4–3.0 log CFU/mL at the highest tested concentration. No significant differences in bacterial loads within MRSA biofilms were observed between the various implant materials, upon exposure to increasing concentrations of antibiotics.DiscussionThe surface parameters of MRSA biofilms were determined by those of the implant materials on which they were formed. The antibiotic susceptibility of MRSA biofilms on the various tested implant materials did not differ, indicating that the efficacy of antibiotics was not affected by the roughness of the biofilm.
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spelling doaj.art-b2a26b91cbf14ef08ea41b6078f3352d2023-04-20T17:26:10ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-04-011410.3389/fmicb.2023.11452101145210Influence of surface characteristics of implant materials on MRSA biofilm formation and effects of antimicrobial treatmentSven C. J. van Dun0Mariëlle Verheul1Bart G. C. W. Pijls2Joffrey van Prehn3Henk Scheper4Federica Galli5Peter H. Nibbering6Mark G. J. de Boer7Department of Infectious Diseases, Leiden University Medical Center, Leiden, NetherlandsDepartment of Infectious Diseases, Leiden University Medical Center, Leiden, NetherlandsDepartment of Orthopedics, Leiden University Medical Center, Leiden, NetherlandsDepartment of Medical Microbiology, Leiden University Medical Center, Leiden, NetherlandsDepartment of Infectious Diseases, Leiden University Medical Center, Leiden, NetherlandsLeiden Institute of Physics, Leiden, NetherlandsDepartment of Infectious Diseases, Leiden University Medical Center, Leiden, NetherlandsDepartment of Infectious Diseases, Leiden University Medical Center, Leiden, NetherlandsIntroductionOne of the main causes of treatment failure in bacterial prosthetic joint infections (PJI) is biofilm formation. The topography of the biofilm may be associated with susceptibility to antimicrobial treatment. The aims of this study were to assess differences in topography of biofilms on different implant materials and the correlation thereof with susceptibility to antimicrobial treatment.MethodsMethicillin-resistant Staphylococcus aureus (MRSA) 7-day mature biofilms were generated on disks made from titanium alloys (Ti-6Al-7Nb and Ti-6Al-4V), synthetic polymer and orthopedic bone cement, commonly used in implant surgery. The surface topography of these implant materials and the biofilms cultured on them was assessed using atomic force microscopy. This provided detailed images, as well as average roughness (Ra) and peak-to-valley roughness (Rt) values in nanometers, of the biofilm and the material surfaces. Bacterial counts within biofilms were assessed microbiologically. Antimicrobial treatment of biofilms was performed by 24-h exposure to the combination of rifampicin and ciprofloxacin in concentrations of 1-, 5- and 10-times the minimal bactericidal concentration (MBC). Finally, treatment-induced differences in bacterial loads and their correlation with biofilm surface parameters were assessed.ResultsThe biofilm surfaces on titanium alloys Ti-6Al-7Nb (Ra = 186 nm) and Ti-6Al-4V (Ra = 270 nm) were less rough than those of biofilms on silicone (Ra = 636 nm). The highest roughness was observed for biofilms on orthopedic bone cement with an Ra of 1,551 nm. Interestingly, the roughness parameters of the titanium alloys themselves were lower than the value for silicone, whereas the surface of the bone cement was the roughest. Treatment with 1- and 5-times the MBC of antibiotics resulted in inter-material differences in colony forming units (CFU) counts, ultimately showing comparable reductions of 2.4–3.0 log CFU/mL at the highest tested concentration. No significant differences in bacterial loads within MRSA biofilms were observed between the various implant materials, upon exposure to increasing concentrations of antibiotics.DiscussionThe surface parameters of MRSA biofilms were determined by those of the implant materials on which they were formed. The antibiotic susceptibility of MRSA biofilms on the various tested implant materials did not differ, indicating that the efficacy of antibiotics was not affected by the roughness of the biofilm.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1145210/fullPJIStaphylococcus aureusMRSAbiofilmatomic force microscopy (AFM)
spellingShingle Sven C. J. van Dun
Mariëlle Verheul
Bart G. C. W. Pijls
Joffrey van Prehn
Henk Scheper
Federica Galli
Peter H. Nibbering
Mark G. J. de Boer
Influence of surface characteristics of implant materials on MRSA biofilm formation and effects of antimicrobial treatment
Frontiers in Microbiology
PJI
Staphylococcus aureus
MRSA
biofilm
atomic force microscopy (AFM)
title Influence of surface characteristics of implant materials on MRSA biofilm formation and effects of antimicrobial treatment
title_full Influence of surface characteristics of implant materials on MRSA biofilm formation and effects of antimicrobial treatment
title_fullStr Influence of surface characteristics of implant materials on MRSA biofilm formation and effects of antimicrobial treatment
title_full_unstemmed Influence of surface characteristics of implant materials on MRSA biofilm formation and effects of antimicrobial treatment
title_short Influence of surface characteristics of implant materials on MRSA biofilm formation and effects of antimicrobial treatment
title_sort influence of surface characteristics of implant materials on mrsa biofilm formation and effects of antimicrobial treatment
topic PJI
Staphylococcus aureus
MRSA
biofilm
atomic force microscopy (AFM)
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1145210/full
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