Real time monitoring of Staphylococcus aureus biofilm sensitivity towards antibiotics with isothermal microcalorimetry

Biofilm-associated infections with Staphylococcus aureus are difficult to treat even after administration of antibiotics that according to the standard susceptibility assays are effective. Currently, the assays used in the clinical laboratories to determine the sensitivity of S . aureus towards anti...

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Vydáno v:PloS one Ročník 17; číslo 2; s. e0260272
Hlavní autoři: Sultan, Andi Rofian, Tavakol, Mehri, Lemmens-den Toom, Nicole A., Croughs, Peter D., Verkaik, Nelianne J., Verbon, Annelies, van Wamel, Willem J. B.
Médium: Journal Article
Jazyk:angličtina
Vydáno: United States Public Library of Science 16.02.2022
Public Library of Science (PLoS)
Témata:
Anti-Bacterial Agents - pharmacology
Antibiotic resistance
Antibiotics
Assaying
Bacteria
Biofilms
Biofilms - drug effects
Biology and Life Sciences
Calorimetry
Calorimetry - methods
Care and treatment
Cefotaxime
Cefuroxime
Clindamycin
Cotrimoxazole
Diagnosis
Dilution
Doxycycline
Drug resistance
Drug resistance in microorganisms
Erythromycin
Evaluation
Extracellular matrix
Floxacillin - pharmacology
Flucloxacillin
Fusidic acid
Genetic Linkage
Gentamicin
Infectious diseases
Levofloxacin
Linezolid
Medicine and Health Sciences
Metabolism
Methicillin
Methicillin-Resistant Staphylococcus aureus - genetics
Methicillin-Resistant Staphylococcus aureus - physiology
Microbial Sensitivity Tests
Monitoring
Penicillin
Real time
Rifampin
Rifampin - pharmacology
Sensitivity
Staphylococcus aureus
Staphylococcus aureus - genetics
Staphylococcus aureus - physiology
Staphylococcus aureus infections
Staphylococcus infections
Statistical analysis
Strains (organisms)
Vancomycin
Vancomycin - pharmacology
United States
United States > US
Sweden
Netherlands
ISSN:1932-6203, 1932-6203
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Abstract Biofilm-associated infections with Staphylococcus aureus are difficult to treat even after administration of antibiotics that according to the standard susceptibility assays are effective. Currently, the assays used in the clinical laboratories to determine the sensitivity of S . aureus towards antibiotics are not representing the behaviour of biofilm-associated S . aureus , since these assays are performed on planktonic bacteria. In research settings, microcalorimetry has been used for antibiotic susceptibility studies. Therefore, in this study we investigated if we can use isothermal microcalorimetry to monitor the response of biofilm towards antibiotic treatment in real-time. We developed a reproducible method to generate biofilm in an isothermal microcalorimeter setup. Using this system, the sensitivity of 5 methicillin-sensitive S . aureus (MSSA) and 5 methicillin-resistant S . aureus (MRSA) strains from different genetic lineages were determined towards: flucloxacillin, cefuroxime, cefotaxime, gentamicin, rifampicin, vancomycin, levofloxacin, clindamycin, erythromycin, linezolid, fusidic acid, co-trimoxazole, and doxycycline. In contrast to conventional assays, our calorimetry-based biofilm susceptibility assay showed that S . aureus biofilms, regardless MSSA or MRSA, can survive the exposure to the maximum serum concentration of all tested antibiotics. The only treatment with a single antibiotic showing a significant reduction in biofilm survival was rifampicin, yet in 20% of the strains, emerging antibiotic resistance was observed. Furthermore, the combination of rifampicin with flucloxacillin, vancomycin or levofloxacin was able to prevent S . aureus biofilm from becoming resistant to rifampicin. Isothermal microcalorimetry allows real-time monitoring of the sensitivity of S . aureus biofilms towards antibiotics in a fast and reliable way.
AbstractList Biofilm-associated infections with Staphylococcus aureus are difficult to treat even after administration of antibiotics that according to the standard susceptibility assays are effective. Currently, the assays used in the clinical laboratories to determine the sensitivity of S. aureus towards antibiotics are not representing the behaviour of biofilm-associated S. aureus, since these assays are performed on planktonic bacteria. In research settings, microcalorimetry has been used for antibiotic susceptibility studies. Therefore, in this study we investigated if we can use isothermal microcalorimetry to monitor the response of biofilm towards antibiotic treatment in real-time. We developed a reproducible method to generate biofilm in an isothermal microcalorimeter setup. Using this system, the sensitivity of 5 methicillin-sensitive S. aureus (MSSA) and 5 methicillin-resistant S. aureus (MRSA) strains from different genetic lineages were determined towards: flucloxacillin, cefuroxime, cefotaxime, gentamicin, rifampicin, vancomycin, levofloxacin, clindamycin, erythromycin, linezolid, fusidic acid, co-trimoxazole, and doxycycline. In contrast to conventional assays, our calorimetry-based biofilm susceptibility assay showed that S. aureus biofilms, regardless MSSA or MRSA, can survive the exposure to the maximum serum concentration of all tested antibiotics. The only treatment with a single antibiotic showing a significant reduction in biofilm survival was rifampicin, yet in 20% of the strains, emerging antibiotic resistance was observed. Furthermore, the combination of rifampicin with flucloxacillin, vancomycin or levofloxacin was able to prevent S. aureus biofilm from becoming resistant to rifampicin. Isothermal microcalorimetry allows real-time monitoring of the sensitivity of S. aureus biofilms towards antibiotics in a fast and reliable way.
Biofilm-associated infections with Staphylococcus aureus are difficult to treat even after administration of antibiotics that according to the standard susceptibility assays are effective. Currently, the assays used in the clinical laboratories to determine the sensitivity of S . aureus towards antibiotics are not representing the behaviour of biofilm-associated S . aureus , since these assays are performed on planktonic bacteria. In research settings, microcalorimetry has been used for antibiotic susceptibility studies. Therefore, in this study we investigated if we can use isothermal microcalorimetry to monitor the response of biofilm towards antibiotic treatment in real-time. We developed a reproducible method to generate biofilm in an isothermal microcalorimeter setup. Using this system, the sensitivity of 5 methicillin-sensitive S . aureus (MSSA) and 5 methicillin-resistant S . aureus (MRSA) strains from different genetic lineages were determined towards: flucloxacillin, cefuroxime, cefotaxime, gentamicin, rifampicin, vancomycin, levofloxacin, clindamycin, erythromycin, linezolid, fusidic acid, co-trimoxazole, and doxycycline. In contrast to conventional assays, our calorimetry-based biofilm susceptibility assay showed that S . aureus biofilms, regardless MSSA or MRSA, can survive the exposure to the maximum serum concentration of all tested antibiotics. The only treatment with a single antibiotic showing a significant reduction in biofilm survival was rifampicin, yet in 20% of the strains, emerging antibiotic resistance was observed. Furthermore, the combination of rifampicin with flucloxacillin, vancomycin or levofloxacin was able to prevent S . aureus biofilm from becoming resistant to rifampicin. Isothermal microcalorimetry allows real-time monitoring of the sensitivity of S . aureus biofilms towards antibiotics in a fast and reliable way.
Biofilm-associated infections with Staphylococcus aureus are difficult to treat even after administration of antibiotics that according to the standard susceptibility assays are effective. Currently, the assays used in the clinical laboratories to determine the sensitivity of S. aureus towards antibiotics are not representing the behaviour of biofilm-associated S. aureus, since these assays are performed on planktonic bacteria. In research settings, microcalorimetry has been used for antibiotic susceptibility studies. Therefore, in this study we investigated if we can use isothermal microcalorimetry to monitor the response of biofilm towards antibiotic treatment in real-time. We developed a reproducible method to generate biofilm in an isothermal microcalorimeter setup. Using this system, the sensitivity of 5 methicillin-sensitive S. aureus (MSSA) and 5 methicillin-resistant S. aureus (MRSA) strains from different genetic lineages were determined towards: flucloxacillin, cefuroxime, cefotaxime, gentamicin, rifampicin, vancomycin, levofloxacin, clindamycin, erythromycin, linezolid, fusidic acid, co-trimoxazole, and doxycycline. In contrast to conventional assays, our calorimetry-based biofilm susceptibility assay showed that S. aureus biofilms, regardless MSSA or MRSA, can survive the exposure to the maximum serum concentration of all tested antibiotics. The only treatment with a single antibiotic showing a significant reduction in biofilm survival was rifampicin, yet in 20% of the strains, emerging antibiotic resistance was observed. Furthermore, the combination of rifampicin with flucloxacillin, vancomycin or levofloxacin was able to prevent S. aureus biofilm from becoming resistant to rifampicin. Isothermal microcalorimetry allows real-time monitoring of the sensitivity of S. aureus biofilms towards antibiotics in a fast and reliable way.Biofilm-associated infections with Staphylococcus aureus are difficult to treat even after administration of antibiotics that according to the standard susceptibility assays are effective. Currently, the assays used in the clinical laboratories to determine the sensitivity of S. aureus towards antibiotics are not representing the behaviour of biofilm-associated S. aureus, since these assays are performed on planktonic bacteria. In research settings, microcalorimetry has been used for antibiotic susceptibility studies. Therefore, in this study we investigated if we can use isothermal microcalorimetry to monitor the response of biofilm towards antibiotic treatment in real-time. We developed a reproducible method to generate biofilm in an isothermal microcalorimeter setup. Using this system, the sensitivity of 5 methicillin-sensitive S. aureus (MSSA) and 5 methicillin-resistant S. aureus (MRSA) strains from different genetic lineages were determined towards: flucloxacillin, cefuroxime, cefotaxime, gentamicin, rifampicin, vancomycin, levofloxacin, clindamycin, erythromycin, linezolid, fusidic acid, co-trimoxazole, and doxycycline. In contrast to conventional assays, our calorimetry-based biofilm susceptibility assay showed that S. aureus biofilms, regardless MSSA or MRSA, can survive the exposure to the maximum serum concentration of all tested antibiotics. The only treatment with a single antibiotic showing a significant reduction in biofilm survival was rifampicin, yet in 20% of the strains, emerging antibiotic resistance was observed. Furthermore, the combination of rifampicin with flucloxacillin, vancomycin or levofloxacin was able to prevent S. aureus biofilm from becoming resistant to rifampicin. Isothermal microcalorimetry allows real-time monitoring of the sensitivity of S. aureus biofilms towards antibiotics in a fast and reliable way.
Audience Academic
Author Lemmens-den Toom, Nicole A.
Croughs, Peter D.
van Wamel, Willem J. B.
Verkaik, Nelianne J.
Verbon, Annelies
Sultan, Andi Rofian
Tavakol, Mehri
AuthorAffiliation 1 Department of Medical Microbiology and Infectious Diseases, Erasmus University Medical Center, Rotterdam, The Netherlands
2 Department of Microbiology, Faculty of Medicine, Hasanuddin University, Makassar, Indonesia
Universidade Nova de Lisboa, PORTUGAL
AuthorAffiliation_xml – name: Universidade Nova de Lisboa, PORTUGAL
– name: 2 Department of Microbiology, Faculty of Medicine, Hasanuddin University, Makassar, Indonesia
– name: 1 Department of Medical Microbiology and Infectious Diseases, Erasmus University Medical Center, Rotterdam, The Netherlands
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  givenname: Andi Rofian
  surname: Sultan
  fullname: Sultan, Andi Rofian
– sequence: 2
  givenname: Mehri
  surname: Tavakol
  fullname: Tavakol, Mehri
– sequence: 3
  givenname: Nicole A.
  surname: Lemmens-den Toom
  fullname: Lemmens-den Toom, Nicole A.
– sequence: 4
  givenname: Peter D.
  surname: Croughs
  fullname: Croughs, Peter D.
– sequence: 5
  givenname: Nelianne J.
  surname: Verkaik
  fullname: Verkaik, Nelianne J.
– sequence: 6
  givenname: Annelies
  surname: Verbon
  fullname: Verbon, Annelies
– sequence: 7
  givenname: Willem J. B.
  surname: van Wamel
  fullname: van Wamel, Willem J. B.
BackLink https://www.ncbi.nlm.nih.gov/pubmed/35171906$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright COPYRIGHT 2022 Public Library of Science
2022 Sultan et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
2022 Sultan et al 2022 Sultan et al
Copyright_xml – notice: COPYRIGHT 2022 Public Library of Science
– notice: 2022 Sultan et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
– notice: 2022 Sultan et al 2022 Sultan et al
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Snippet Biofilm-associated infections with Staphylococcus aureus are difficult to treat even after administration of antibiotics that according to the standard...
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SubjectTerms Anti-Bacterial Agents - pharmacology
Antibiotic resistance
Antibiotics
Assaying
Bacteria
Biofilms
Biofilms - drug effects
Biology and Life Sciences
Calorimetry
Calorimetry - methods
Care and treatment
Cefotaxime
Cefuroxime
Clindamycin
Cotrimoxazole
Diagnosis
Dilution
Doxycycline
Drug resistance
Drug resistance in microorganisms
Erythromycin
Evaluation
Extracellular matrix
Floxacillin - pharmacology
Flucloxacillin
Fusidic acid
Genetic Linkage
Gentamicin
Infectious diseases
Levofloxacin
Linezolid
Medicine and Health Sciences
Metabolism
Methicillin
Methicillin-Resistant Staphylococcus aureus - genetics
Methicillin-Resistant Staphylococcus aureus - physiology
Microbial Sensitivity Tests
Monitoring
Penicillin
Real time
Rifampin
Rifampin - pharmacology
Sensitivity
Staphylococcus aureus
Staphylococcus aureus - genetics
Staphylococcus aureus - physiology
Staphylococcus aureus infections
Staphylococcus infections
Statistical analysis
Strains (organisms)
Vancomycin
Vancomycin - pharmacology
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Title Real time monitoring of Staphylococcus aureus biofilm sensitivity towards antibiotics with isothermal microcalorimetry
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