Genomics of Staphylococcus aureus and Staphylococcus epidermidis from Periprosthetic Joint Infections and Correlation to Clinical Outcome

ABSTRACT The approach of sequencing or genotyping to characterize the pathogenic potential of staphylococci from orthopedic device-related infection (ODRI) has been applied in recent studies. These studies described the genomic carriage of virulence in clinical strains and compared it with those in...

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Main Authors: Margarita Trobos, Rininta Firdaus, Karin Svensson Malchau, Jonatan Tillander, Dimitrios Arnellos, Ola Rolfson, Peter Thomsen, Iñigo Lasa
Format: Article
Language:English
Published: American Society for Microbiology 2022-08-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.02181-21
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author Margarita Trobos
Rininta Firdaus
Karin Svensson Malchau
Jonatan Tillander
Dimitrios Arnellos
Ola Rolfson
Peter Thomsen
Iñigo Lasa
author_facet Margarita Trobos
Rininta Firdaus
Karin Svensson Malchau
Jonatan Tillander
Dimitrios Arnellos
Ola Rolfson
Peter Thomsen
Iñigo Lasa
author_sort Margarita Trobos
collection DOAJ
description ABSTRACT The approach of sequencing or genotyping to characterize the pathogenic potential of staphylococci from orthopedic device-related infection (ODRI) has been applied in recent studies. These studies described the genomic carriage of virulence in clinical strains and compared it with those in commensal strains. Only a few studies have directly correlated genomic profiles to patient outcome and phenotypic virulence properties in periprosthetic joint infections (PJIs). We investigated the association between genomic variations and virulence-associated phenotypes (biofilm-forming ability and antimicrobial resistance) in 111 staphylococcal strains isolated from patients with PJI and the infection outcome (resolved/unresolved). The presence of a strong biofilm phenotype in Staphylococcus aureus and an antibiotic-resistant phenotype in Staphylococcus epidermidis were both associated with treatment failure of PJI. In S. epidermidis, multidrug resistance (MDR) and resistance to rifampicin were associated with unresolved infection. Sequence type 45 (ST45) and ST2 were particularly enriched in S. aureus and S. epidermidis, respectively. S. epidermidis ST2 caused the majority of relapses and was associated with MDR and strong biofilm production, whereas ST215 correlated with MDR and non/weak biofilm production. S. aureus agr II correlated with resolved infection, while S. epidermidis agr I was associated with strong biofilm production and agr III with non/weak production. Collectively, our results highlight the importance of careful genomic and phenotypic characterization to anticipate the probability of the strain causing treatment failure in PJI. Due to the high rate of resistant S. epidermidis strains identified, this study provides evidence that the current recommended treatment of rifampicin and a fluoroquinolone should not be administered without knowledge of the resistance pattern. IMPORTANCE This study addresses the presence and frequency of particular genetic variants and virulence factors found in staphylococcal bacteria causing periprosthetic joint infection (PJI) of the hip and knee to ascertain their clinical relevance as predictors of treatment failure. We characterized the genetic virulence traits of a large collection of clinical staphylococci isolated from patients with PJI and evaluated their association with the patient’s infection outcome. The results showed that S. aureus strains that produced strong biofilms and S. epidermidis strains with resistance to several antibiotics associated significantly with unresolved infection. Some particular genetic variants associated with biofilm formation and multidrug resistance. These traits should be considered important risk factors for the diagnosis and treatment guidance in PJI.
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spelling doaj.art-24adac7a7b864c33a5793ad415f6f40e2022-12-22T03:44:53ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-08-0110410.1128/spectrum.02181-21Genomics of Staphylococcus aureus and Staphylococcus epidermidis from Periprosthetic Joint Infections and Correlation to Clinical OutcomeMargarita Trobos0Rininta Firdaus1Karin Svensson Malchau2Jonatan Tillander3Dimitrios Arnellos4Ola Rolfson5Peter Thomsen6Iñigo Lasa7Department of Biomaterials, Institute of Clinical Sciences, Sahlgrenska Academy, University of Gothenburg, Gothenburg, SwedenDepartment of Biomaterials, Institute of Clinical Sciences, Sahlgrenska Academy, University of Gothenburg, Gothenburg, SwedenCenter for Antibiotic Resistance Research (CARe), University of Gothenburg, Gothenburg, SwedenCenter for Antibiotic Resistance Research (CARe), University of Gothenburg, Gothenburg, Sweden1928 Diagnostics, Gothenburg, SwedenDepartment of Orthopedics, Institute of Clinical Sciences, Sahlgrenska Academy, University of Gothenburg, Gothenburg, SwedenDepartment of Biomaterials, Institute of Clinical Sciences, Sahlgrenska Academy, University of Gothenburg, Gothenburg, SwedenLaboratory of Microbial Pathogenesis, Navarrabiomed, Hospital Universitario de Navarra (HUN), Universidad Pública de Navarra (UPNA), IdiSNA, Pamplona, SpainABSTRACT The approach of sequencing or genotyping to characterize the pathogenic potential of staphylococci from orthopedic device-related infection (ODRI) has been applied in recent studies. These studies described the genomic carriage of virulence in clinical strains and compared it with those in commensal strains. Only a few studies have directly correlated genomic profiles to patient outcome and phenotypic virulence properties in periprosthetic joint infections (PJIs). We investigated the association between genomic variations and virulence-associated phenotypes (biofilm-forming ability and antimicrobial resistance) in 111 staphylococcal strains isolated from patients with PJI and the infection outcome (resolved/unresolved). The presence of a strong biofilm phenotype in Staphylococcus aureus and an antibiotic-resistant phenotype in Staphylococcus epidermidis were both associated with treatment failure of PJI. In S. epidermidis, multidrug resistance (MDR) and resistance to rifampicin were associated with unresolved infection. Sequence type 45 (ST45) and ST2 were particularly enriched in S. aureus and S. epidermidis, respectively. S. epidermidis ST2 caused the majority of relapses and was associated with MDR and strong biofilm production, whereas ST215 correlated with MDR and non/weak biofilm production. S. aureus agr II correlated with resolved infection, while S. epidermidis agr I was associated with strong biofilm production and agr III with non/weak production. Collectively, our results highlight the importance of careful genomic and phenotypic characterization to anticipate the probability of the strain causing treatment failure in PJI. Due to the high rate of resistant S. epidermidis strains identified, this study provides evidence that the current recommended treatment of rifampicin and a fluoroquinolone should not be administered without knowledge of the resistance pattern. IMPORTANCE This study addresses the presence and frequency of particular genetic variants and virulence factors found in staphylococcal bacteria causing periprosthetic joint infection (PJI) of the hip and knee to ascertain their clinical relevance as predictors of treatment failure. We characterized the genetic virulence traits of a large collection of clinical staphylococci isolated from patients with PJI and evaluated their association with the patient’s infection outcome. The results showed that S. aureus strains that produced strong biofilms and S. epidermidis strains with resistance to several antibiotics associated significantly with unresolved infection. Some particular genetic variants associated with biofilm formation and multidrug resistance. These traits should be considered important risk factors for the diagnosis and treatment guidance in PJI.https://journals.asm.org/doi/10.1128/spectrum.02181-21Staphylococcusperiprosthetic joint infectionbiofilmantibiotic resistancevirulencepatient outcome
spellingShingle Margarita Trobos
Rininta Firdaus
Karin Svensson Malchau
Jonatan Tillander
Dimitrios Arnellos
Ola Rolfson
Peter Thomsen
Iñigo Lasa
Genomics of Staphylococcus aureus and Staphylococcus epidermidis from Periprosthetic Joint Infections and Correlation to Clinical Outcome
Microbiology Spectrum
Staphylococcus
periprosthetic joint infection
biofilm
antibiotic resistance
virulence
patient outcome
title Genomics of Staphylococcus aureus and Staphylococcus epidermidis from Periprosthetic Joint Infections and Correlation to Clinical Outcome
title_full Genomics of Staphylococcus aureus and Staphylococcus epidermidis from Periprosthetic Joint Infections and Correlation to Clinical Outcome
title_fullStr Genomics of Staphylococcus aureus and Staphylococcus epidermidis from Periprosthetic Joint Infections and Correlation to Clinical Outcome
title_full_unstemmed Genomics of Staphylococcus aureus and Staphylococcus epidermidis from Periprosthetic Joint Infections and Correlation to Clinical Outcome
title_short Genomics of Staphylococcus aureus and Staphylococcus epidermidis from Periprosthetic Joint Infections and Correlation to Clinical Outcome
title_sort genomics of staphylococcus aureus and staphylococcus epidermidis from periprosthetic joint infections and correlation to clinical outcome
topic Staphylococcus
periprosthetic joint infection
biofilm
antibiotic resistance
virulence
patient outcome
url https://journals.asm.org/doi/10.1128/spectrum.02181-21
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