Biofilm and the effect of sonication in a chronic Staphylococcus epidermidis orthopedic in vivo implant infection model

Abstract Background In diagnosing chronic orthopedic implant infections culture of sonicate represents a supplement to tissue cultures. However, the extent to which biofilm forms on implant surfaces and the degree of dislodgement of bacteria by sonication remains unclear. In this in vivo study using...

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Main Authors: Erik Thorvaldsen Sandbakken, Erling Høyer, Eivind Witsø, Caroline Krogh Søgaard, Alberto Díez-Sánchez, Linh Hoang, Tina Strømdal Wik, Kåre Bergh
Format: Article
Language:English
Published: BMC 2024-12-01
Series:Journal of Orthopaedic Surgery and Research
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Online Access:https://doi.org/10.1186/s13018-024-05309-3
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author Erik Thorvaldsen Sandbakken
Erling Høyer
Eivind Witsø
Caroline Krogh Søgaard
Alberto Díez-Sánchez
Linh Hoang
Tina Strømdal Wik
Kåre Bergh
author_facet Erik Thorvaldsen Sandbakken
Erling Høyer
Eivind Witsø
Caroline Krogh Søgaard
Alberto Díez-Sánchez
Linh Hoang
Tina Strømdal Wik
Kåre Bergh
author_sort Erik Thorvaldsen Sandbakken
collection DOAJ
description Abstract Background In diagnosing chronic orthopedic implant infections culture of sonicate represents a supplement to tissue cultures. However, the extent to which biofilm forms on implant surfaces and the degree of dislodgement of bacteria by sonication remains unclear. In this in vivo study using a low bacterial inoculum, we aimed to determine whether a variable effect of sonication could be observed in a standardized in vivo model. Materials and Methods Seven Wistar rats underwent surgery with intramuscular implantation of two bone xenograft implants, each containing two steel plates. The grafts were inoculated with approximately 500 colony forming units (CFU) of Staphylococcus epidermidis ATCC 35984. After 20 days the rats were sacrificed, and the steel plates were removed from the bone grafts. Epifluorescence microscopy and scanning electron microscopy (SEM) were used to visualize biofilm formation and dislodgement on the plate surfaces. In addition to cultures of sonicate, a quantitative S. epidermidis specific PCR was developed for enumeration of bacteria. Results A chronic, low-grade implant infection was successfully established, with all animals remaining in good health. All infected bone graft implants yielded abundant growth of S. epidermidis, with a median of 3.25 (1.6–4.6) × 10⁷ CFU per/graft. We were unable to distinguish infected plates from negative controls using epifluorescence microscopy. On infected plates small colonies of staphylococci were identified by SEM. The number of bacteria detected in the sonicate was low with 500 (100–2400) CFU/plate and 475 (140–1821) copies/plate by qPCR. The difference in area covered by fluorescent material before and after sonication was 10.1 (5.7–12.3) %, p = 0.018. Conclusion Despite the pronounced infection in the surrounding tissue, only few bacteria were detected on the surface of the steel implants. This is evident from the minimal findings by SEM before sonication, as well as the very low CFU counts and DNA copies in the sonicate. Sonication did not show variable effectiveness, indicating it is a valuable addition to, but not a replacement for biopsy cultures in cases of implant-associated infections with low-virulence microorganisms.
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spelling doaj-art-59ea5e43b6d643fe95b543b8e45bbc462025-08-20T02:31:04ZengBMCJournal of Orthopaedic Surgery and Research1749-799X2024-12-0119111410.1186/s13018-024-05309-3Biofilm and the effect of sonication in a chronic Staphylococcus epidermidis orthopedic in vivo implant infection modelErik Thorvaldsen Sandbakken0Erling Høyer1Eivind Witsø2Caroline Krogh Søgaard3Alberto Díez-Sánchez4Linh Hoang5Tina Strømdal Wik6Kåre Bergh7Department of Orthopedic Surgery, St. Olavs HospitalDepartement of Medical Microbiology, St. Olavs HospitalDepartment of Orthopedic Surgery, St. Olavs HospitalDepartment of Clinical and Molecular Medicine, NTNUCellular and Molecular Imaging Core Facility (CMIC), NTNUCellular and Molecular Imaging Core Facility (CMIC), NTNUDepartment of Orthopedic Surgery, St. Olavs HospitalDepartement of Medical Microbiology, St. Olavs HospitalAbstract Background In diagnosing chronic orthopedic implant infections culture of sonicate represents a supplement to tissue cultures. However, the extent to which biofilm forms on implant surfaces and the degree of dislodgement of bacteria by sonication remains unclear. In this in vivo study using a low bacterial inoculum, we aimed to determine whether a variable effect of sonication could be observed in a standardized in vivo model. Materials and Methods Seven Wistar rats underwent surgery with intramuscular implantation of two bone xenograft implants, each containing two steel plates. The grafts were inoculated with approximately 500 colony forming units (CFU) of Staphylococcus epidermidis ATCC 35984. After 20 days the rats were sacrificed, and the steel plates were removed from the bone grafts. Epifluorescence microscopy and scanning electron microscopy (SEM) were used to visualize biofilm formation and dislodgement on the plate surfaces. In addition to cultures of sonicate, a quantitative S. epidermidis specific PCR was developed for enumeration of bacteria. Results A chronic, low-grade implant infection was successfully established, with all animals remaining in good health. All infected bone graft implants yielded abundant growth of S. epidermidis, with a median of 3.25 (1.6–4.6) × 10⁷ CFU per/graft. We were unable to distinguish infected plates from negative controls using epifluorescence microscopy. On infected plates small colonies of staphylococci were identified by SEM. The number of bacteria detected in the sonicate was low with 500 (100–2400) CFU/plate and 475 (140–1821) copies/plate by qPCR. The difference in area covered by fluorescent material before and after sonication was 10.1 (5.7–12.3) %, p = 0.018. Conclusion Despite the pronounced infection in the surrounding tissue, only few bacteria were detected on the surface of the steel implants. This is evident from the minimal findings by SEM before sonication, as well as the very low CFU counts and DNA copies in the sonicate. Sonication did not show variable effectiveness, indicating it is a valuable addition to, but not a replacement for biopsy cultures in cases of implant-associated infections with low-virulence microorganisms.https://doi.org/10.1186/s13018-024-05309-3BiofilmAnimal modelImplant infection modelStaphylococcus epidermidisSonicationPCR
spellingShingle Erik Thorvaldsen Sandbakken
Erling Høyer
Eivind Witsø
Caroline Krogh Søgaard
Alberto Díez-Sánchez
Linh Hoang
Tina Strømdal Wik
Kåre Bergh
Biofilm and the effect of sonication in a chronic Staphylococcus epidermidis orthopedic in vivo implant infection model
Journal of Orthopaedic Surgery and Research
Biofilm
Animal model
Implant infection model
Staphylococcus epidermidis
Sonication
PCR
title Biofilm and the effect of sonication in a chronic Staphylococcus epidermidis orthopedic in vivo implant infection model
title_full Biofilm and the effect of sonication in a chronic Staphylococcus epidermidis orthopedic in vivo implant infection model
title_fullStr Biofilm and the effect of sonication in a chronic Staphylococcus epidermidis orthopedic in vivo implant infection model
title_full_unstemmed Biofilm and the effect of sonication in a chronic Staphylococcus epidermidis orthopedic in vivo implant infection model
title_short Biofilm and the effect of sonication in a chronic Staphylococcus epidermidis orthopedic in vivo implant infection model
title_sort biofilm and the effect of sonication in a chronic staphylococcus epidermidis orthopedic in vivo implant infection model
topic Biofilm
Animal model
Implant infection model
Staphylococcus epidermidis
Sonication
PCR
url https://doi.org/10.1186/s13018-024-05309-3
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