Comparative genomic analysis of resistance and virulence genes in staphylococcus epidermidis and their impact on clinical outcome of musculoskeletal infections
Abstract Staphylococcus epidermidis is an opportunistic commensal cutaneous biofilm-producing agent frequently causing musculoskeletal infections (MSI) with/without implants. This study was design to evaluate phenotypic and genomic relatedness between commensal skin and MSI S. epidermidis isolates a...
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Nature Portfolio
2025-07-01
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| Online Access: | https://doi.org/10.1038/s41598-025-09061-4 |
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| author | Ingrid Nayara Marcelino Santos Felipe Alberto-Lei Fernanda Fernandes Santos Mariana Felix Cerqueira Balera Mariana Neri Kurihara Carolina Coelho Cunha Laís Sales Seriacopi Thomas Stravinskas Durigon Fernando Baldy Reis Ana Karolina Antunes Eisen Giovana Santos Caleiro Jansen de Araújo Edison Luiz Durigon Giselle Burlamaqui Klautau Mauro José Salles |
| author_facet | Ingrid Nayara Marcelino Santos Felipe Alberto-Lei Fernanda Fernandes Santos Mariana Felix Cerqueira Balera Mariana Neri Kurihara Carolina Coelho Cunha Laís Sales Seriacopi Thomas Stravinskas Durigon Fernando Baldy Reis Ana Karolina Antunes Eisen Giovana Santos Caleiro Jansen de Araújo Edison Luiz Durigon Giselle Burlamaqui Klautau Mauro José Salles |
| author_sort | Ingrid Nayara Marcelino Santos |
| collection | DOAJ |
| description | Abstract Staphylococcus epidermidis is an opportunistic commensal cutaneous biofilm-producing agent frequently causing musculoskeletal infections (MSI) with/without implants. This study was design to evaluate phenotypic and genomic relatedness between commensal skin and MSI S. epidermidis isolates and to assess patient-related and microbial markers in the outcome of patients after one-year follow-up. Demographics, clinical data and monomicrobial S. epidermidis isolates of MSI patients (n = 31) and healthy individuals (n = 15) were analyzed. Phenotypic profile was assessed by susceptibility tests by broth microdilution and biofilm formation. Phylogenetic relationships, resistome characterization, and virulome analysis were carried out by complete genome sequencing (n = 46). Overall, MSI-derived isolates were significantly more strong/moderate biofilm producers and depicted higher rates of resistance to methicillin (MRSE), ciprofloxacin, gentamicin and rifampicin. Demographics and clinical characteristics did not significantly affect MSI patients’ outcomes. In the whole-genomic sequencing (WGS) phylogeny, most MSI-derived isolates were grouped into the pathogenic-associated clonal complex CC2, and significantly higher prevalence of mecA gene and pathogenic marker IS256. Following multivariate analysis, MSI-derived isolates carrying transposable element IS256 are more likely to develop a persistent infection (odds ratio [OR], 8.00, [95% confidence interval (CI), 1.06 to 60.31], P = 0.044), while weaker biofilm producer were protectors (OR, 0.070, 95%CI, 0.005–0.979, P = 0.048), reducing the chance of recurrence by 93% (1–0.070). The logistic regression model’s performance was evaluated by Nagelkerke’s R, which resulted in 47.21%. In conclusion, S. epidermidis isolates producing MSI were phenotypically and genetically distinct from commensals, proven the association between independent genetic traits and patient’s outcome. |
| format | Article |
| id | doaj-art-2c0f4e52654d44f8b7bda112ab6b0ed7 |
| institution | Kabale University |
| issn | 2045-2322 |
| language | English |
| publishDate | 2025-07-01 |
| publisher | Nature Portfolio |
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| spelling | doaj-art-2c0f4e52654d44f8b7bda112ab6b0ed72025-08-24T11:18:49ZengNature PortfolioScientific Reports2045-23222025-07-0115111310.1038/s41598-025-09061-4Comparative genomic analysis of resistance and virulence genes in staphylococcus epidermidis and their impact on clinical outcome of musculoskeletal infectionsIngrid Nayara Marcelino Santos0Felipe Alberto-Lei1Fernanda Fernandes Santos2Mariana Felix Cerqueira Balera3Mariana Neri Kurihara4Carolina Coelho Cunha5Laís Sales Seriacopi6Thomas Stravinskas Durigon7Fernando Baldy Reis8Ana Karolina Antunes Eisen9Giovana Santos Caleiro10Jansen de Araújo11Edison Luiz Durigon12Giselle Burlamaqui Klautau13Mauro José Salles14Laboratório Especial de Microbiologia Clínica (LEMC), Departamento de Medicina, Disciplina de Infectologia, Escola Paulista de Medicina (EPM), Universidade Federal de São Paulo (UNIFESP)Laboratório Especial de Microbiologia Clínica (LEMC), Departamento de Medicina, Disciplina de Infectologia, Escola Paulista de Medicina (EPM), Universidade Federal de São Paulo (UNIFESP)Laboratório Especial de Microbiologia Clínica (LEMC), Departamento de Medicina, Disciplina de Infectologia, Escola Paulista de Medicina (EPM), Universidade Federal de São Paulo (UNIFESP)Laboratório Especial de Microbiologia Clínica (LEMC), Departamento de Medicina, Disciplina de Infectologia, Escola Paulista de Medicina (EPM), Universidade Federal de São Paulo (UNIFESP)Laboratório Especial de Microbiologia Clínica (LEMC), Departamento de Medicina, Disciplina de Infectologia, Escola Paulista de Medicina (EPM), Universidade Federal de São Paulo (UNIFESP)Grupo de Infecção Musculoesquelética, Departamento de Ortopedia e Traumatologia, Escola Paulista de Medicina (EPM), Universidade Federal de São Paulo (UNIFESP)Grupo de Infecção Musculoesquelética, Departamento de Ortopedia e Traumatologia, Escola Paulista de Medicina (EPM), Universidade Federal de São Paulo (UNIFESP)Grupo de Infecção Musculoesquelética, Departamento de Ortopedia e Traumatologia, Escola Paulista de Medicina (EPM), Universidade Federal de São Paulo (UNIFESP)Grupo de Infecção Musculoesquelética, Departamento de Ortopedia e Traumatologia, Escola Paulista de Medicina (EPM), Universidade Federal de São Paulo (UNIFESP)Laboratório de Virologia Clínica e Molecular, Departamento de Microbiologia, Universidade de São Paulo (USP)Laboratório de Virologia Clínica e Molecular, Departamento de Microbiologia, Universidade de São Paulo (USP)Laboratório de Virologia Clínica e Molecular, Departamento de Microbiologia, Universidade de São Paulo (USP)Laboratório de Virologia Clínica e Molecular, Departamento de Microbiologia, Universidade de São Paulo (USP)Disciplina de Infectologia, Faculdade de Ciências Médicas da Santa Casa de São PauloLaboratório Especial de Microbiologia Clínica (LEMC), Departamento de Medicina, Disciplina de Infectologia, Escola Paulista de Medicina (EPM), Universidade Federal de São Paulo (UNIFESP)Abstract Staphylococcus epidermidis is an opportunistic commensal cutaneous biofilm-producing agent frequently causing musculoskeletal infections (MSI) with/without implants. This study was design to evaluate phenotypic and genomic relatedness between commensal skin and MSI S. epidermidis isolates and to assess patient-related and microbial markers in the outcome of patients after one-year follow-up. Demographics, clinical data and monomicrobial S. epidermidis isolates of MSI patients (n = 31) and healthy individuals (n = 15) were analyzed. Phenotypic profile was assessed by susceptibility tests by broth microdilution and biofilm formation. Phylogenetic relationships, resistome characterization, and virulome analysis were carried out by complete genome sequencing (n = 46). Overall, MSI-derived isolates were significantly more strong/moderate biofilm producers and depicted higher rates of resistance to methicillin (MRSE), ciprofloxacin, gentamicin and rifampicin. Demographics and clinical characteristics did not significantly affect MSI patients’ outcomes. In the whole-genomic sequencing (WGS) phylogeny, most MSI-derived isolates were grouped into the pathogenic-associated clonal complex CC2, and significantly higher prevalence of mecA gene and pathogenic marker IS256. Following multivariate analysis, MSI-derived isolates carrying transposable element IS256 are more likely to develop a persistent infection (odds ratio [OR], 8.00, [95% confidence interval (CI), 1.06 to 60.31], P = 0.044), while weaker biofilm producer were protectors (OR, 0.070, 95%CI, 0.005–0.979, P = 0.048), reducing the chance of recurrence by 93% (1–0.070). The logistic regression model’s performance was evaluated by Nagelkerke’s R, which resulted in 47.21%. In conclusion, S. epidermidis isolates producing MSI were phenotypically and genetically distinct from commensals, proven the association between independent genetic traits and patient’s outcome.https://doi.org/10.1038/s41598-025-09061-4Coagulase-negative StaphylococciStaphylococcus epidermidisBiofilm productionWhole-genomic sequencingPhylogenymecA gene |
| spellingShingle | Ingrid Nayara Marcelino Santos Felipe Alberto-Lei Fernanda Fernandes Santos Mariana Felix Cerqueira Balera Mariana Neri Kurihara Carolina Coelho Cunha Laís Sales Seriacopi Thomas Stravinskas Durigon Fernando Baldy Reis Ana Karolina Antunes Eisen Giovana Santos Caleiro Jansen de Araújo Edison Luiz Durigon Giselle Burlamaqui Klautau Mauro José Salles Comparative genomic analysis of resistance and virulence genes in staphylococcus epidermidis and their impact on clinical outcome of musculoskeletal infections Scientific Reports Coagulase-negative Staphylococci Staphylococcus epidermidis Biofilm production Whole-genomic sequencing Phylogeny mecA gene |
| title | Comparative genomic analysis of resistance and virulence genes in staphylococcus epidermidis and their impact on clinical outcome of musculoskeletal infections |
| title_full | Comparative genomic analysis of resistance and virulence genes in staphylococcus epidermidis and their impact on clinical outcome of musculoskeletal infections |
| title_fullStr | Comparative genomic analysis of resistance and virulence genes in staphylococcus epidermidis and their impact on clinical outcome of musculoskeletal infections |
| title_full_unstemmed | Comparative genomic analysis of resistance and virulence genes in staphylococcus epidermidis and their impact on clinical outcome of musculoskeletal infections |
| title_short | Comparative genomic analysis of resistance and virulence genes in staphylococcus epidermidis and their impact on clinical outcome of musculoskeletal infections |
| title_sort | comparative genomic analysis of resistance and virulence genes in staphylococcus epidermidis and their impact on clinical outcome of musculoskeletal infections |
| topic | Coagulase-negative Staphylococci Staphylococcus epidermidis Biofilm production Whole-genomic sequencing Phylogeny mecA gene |
| url | https://doi.org/10.1038/s41598-025-09061-4 |
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