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Susceptibility

In Vivo Gentamicin Susceptibility Test for Prevention of Bacterial Biofilms in Bone Tissue and on Implants

Louise Kruse Jensen, Thomas Bjarnsholt, Kasper N. Kragh, Bent Aalbæk, Nicole Lind Henriksen, Sophie Amalie Blirup, Karen Pankoke, Andreas Petersen, Henrik Elvang Jensen
Louise Kruse Jensen
aDepartment of Veterinary and Animal Sciences, University of Copenhagen, Copenhagen, Denmark
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Thomas Bjarnsholt
bCosterton Biofilm Center, Department of Immunology and Microbiology, University of Copenhagen, Copenhagen, Denmark
cDepartment of Clinical Microbiology, Copenhagen University Hospital, Copenhagen, Denmark
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Kasper N. Kragh
bCosterton Biofilm Center, Department of Immunology and Microbiology, University of Copenhagen, Copenhagen, Denmark
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Bent Aalbæk
aDepartment of Veterinary and Animal Sciences, University of Copenhagen, Copenhagen, Denmark
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Nicole Lind Henriksen
aDepartment of Veterinary and Animal Sciences, University of Copenhagen, Copenhagen, Denmark
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Sophie Amalie Blirup
aDepartment of Veterinary and Animal Sciences, University of Copenhagen, Copenhagen, Denmark
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Karen Pankoke
aDepartment of Veterinary and Animal Sciences, University of Copenhagen, Copenhagen, Denmark
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Andreas Petersen
dStatens Serum Institut, Copenhagen, Denmark
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Henrik Elvang Jensen
aDepartment of Veterinary and Animal Sciences, University of Copenhagen, Copenhagen, Denmark
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DOI: 10.1128/AAC.01889-18
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    FIG 1

    In-vitro time-kill study. The results represent the viable count (in number of CFU per milliliter) of Staphylococcus aureus strain S54F9 in the time-kill experiment with different gentamicin concentrations (16, 160, 1,600, 16,000, and 160,000 times the MIC). On the x axis, 0 represents the number of CFU just before gentamicin exposure. The dotted line at a value of 2 CFU/ml on the y axis represents the detection limit.

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    FIG 2

    Results of sonication and histological registrations. (A) The number of bacteria attached to the implants was reduced with the increasing values of the MIC of gentamicin added to the inoculum. (B and C) The width of the peri-implant pathological bone area (PIBA) (B) and the count of neutrophilic granulocytes (C) were increased only in animals inoculated with bacteria and with bacteria plus 160× MIC gentamicin. Single values and the mean and standard error of the mean (SEM) are shown for each group.

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    FIG 3

    Macroscopic bone pathology. Three pigs were inoculated with Staphylococcus aureus and gentamicin at different MICs in the right tibia, followed by insertion of a steel implant. The pigs were euthanized 5 days after inoculation. The tibial bone was sagittally sectioned, and the implant was removed for demonstration of the implant cavity (IC). (A) Pig inoculated with bacteria and 160,000× MIC of gentamicin. No pus was visible, and the implant cavity is regular. (B) Pig inoculated with bacteria and 160× MIC gentamicin. Pus and bone destruction surround the implant cavity. (C) Pig inoculated with bacteria and 1,600× MIC of gentamicin. Although there was less pus than in the image in panel B, the bone contour of the implant cavity was still destroyed (inset).

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    FIG 4

    Microscopic bone pathology. Two were pigs inoculated with Staphylococcus aureus and different MICs of gentamicin in the right tibia, followed by insertion of a steel implant. The pigs were euthanized 5 days after inoculation. The tibial bone was sagittally sectioned, and the implant was removed for demonstration of the implant cavity (IC). (A) Pig inoculated with bacteria and 160× MIC of gentamicin. HE stain was used. The arrow indicates the extension of the peri-implant pathological bone area (PIBA). PIBA contains necrotic bone tissue and a massive infiltration of neutrophilic granulocytes and macrophages. (B) Pig inoculated with bacteria and 160,000× MIC of gentamicin. HE stain was used. PIBA is small (double arrow), and only a sparse inflammatory reaction was present. (C) Close-up of the image in panel A. A microabscess that contained small aggregates of bacteria (arrow) and that was surrounded by multinuclear giant cells is seen. (D) Within the microabscess, S. aureus was detected immunohistochemically. Red positive bacteria (arrow) can be seen among the neutrophilic granulocytes (NG).

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    FIG 5

    Inoculation procedure in a porcine model of implant-associated osteomyelitis. (A) A small incision down to the periosteum was made on the medial side of the proximal right tibia, and a 4-mm K wire (arrow) was drilled 2 cm into the bone to establish the implant cavity. (B) The inoculum containing S. aureus bacteria and different concentrations of gentamicin (arrow) was injected into the implant cavity. (C) After inoculation, a steel implant of 2 by 15 mm (made from a K wire) was inserted into the implant cavity, and the periosteum was closed with sutures (arrow), followed by closure of the soft tissue and skin. (D) Fluoroscopy just after the operation. The implant (arrow) is seen in the implant cavity.

Tables

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  • TABLE 1

    Overview of study groups and detection of bacteria postmortem

    GroupAnimal no.InoculumDetection of bacteria in implant cavity (swab)Detection of biofilm in:
    Implant (sonication)Tissue around implant cavity (IHCa)
    AA1SalineNoNo
    A2SalineNoNo
    A3SalineNoNo
    A4SalineNoNoNo
    A5SalineNoNoNo
    A6SalineNoNoNo
    BB1S. aureusYes (inoculated spa type)YesYes
    B2S. aureusYes (inoculated spa type)YesNo
    B3S. aureusYes (inoculated spa type)YesYes
    B4S. aureusYes (inoculated spa type)YesYes
    B5S. aureusYes (inoculated spa type)YesYes
    B6S. aureusYes (inoculated spa type)YesYes
    CC1S. aureus + 160× MIC (40 mg/liter)Yes (inoculated spa type)YesYes
    C2S. aureus + 160× MICYes (inoculated spa type)YesNo
    C3S. aureus + 160× MICYes (inoculated spa type)YesYes
    DD1S. aureus + 1,600× MIC (400 mg/liter)ContaminationYesNo
    D2S. aureus + 1,600× MICYes (inoculated spa type)YesNo
    D3S. aureus + 1,600× MICYes (inoculated spa type)NoNo
    EE1S. aureus + 16,000× MIC (4,000 mg/liter)NoYesYes
    E2S. aureus + 16,000× MICNoNoNo
    E3S. aureus + 16,000× MICYes (inoculated spa type)YesNo
    FF1S. aureus + 160,000× MIC (40,000 mg/liter)NoNoNo
    F2S. aureus + 160,000× MICYes (inoculated spa type)YesNo
    F3S. aureus + 160,000× MICNoNoNo
    F4S. aureus + 160,000× MICNoNoNo
    • ↵a IHC, immunohistochemistry for S. aureus.

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In Vivo Gentamicin Susceptibility Test for Prevention of Bacterial Biofilms in Bone Tissue and on Implants
Louise Kruse Jensen, Thomas Bjarnsholt, Kasper N. Kragh, Bent Aalbæk, Nicole Lind Henriksen, Sophie Amalie Blirup, Karen Pankoke, Andreas Petersen, Henrik Elvang Jensen
Antimicrobial Agents and Chemotherapy Jan 2019, 63 (2) e01889-18; DOI: 10.1128/AAC.01889-18

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In Vivo Gentamicin Susceptibility Test for Prevention of Bacterial Biofilms in Bone Tissue and on Implants
Louise Kruse Jensen, Thomas Bjarnsholt, Kasper N. Kragh, Bent Aalbæk, Nicole Lind Henriksen, Sophie Amalie Blirup, Karen Pankoke, Andreas Petersen, Henrik Elvang Jensen
Antimicrobial Agents and Chemotherapy Jan 2019, 63 (2) e01889-18; DOI: 10.1128/AAC.01889-18
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    • ABSTRACT
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KEYWORDS

aminoglycosides
animal models
biofilms
susceptibility testing

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