M Bes

Ecole normale supérieure de Lyon, Lyons, Rhône-Alpes, France

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Publications (153)596.31 Total impact

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    ABSTRACT: Using a large collection of European and North-African methicillin-resistant Staphylococcus aureus (MRSA) isolates with a variety of genetic background and SCCmec types, we evaluated the reliability of the BD GeneOhm™ MRSA assay. Results revealed a high performance of this test to detect MRSA strains provided from Europe and North-Africa (98.3%).
    Journal of clinical microbiology. 10/2014;
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    ABSTRACT: SUMMARY Following the recognition of a mecC MRSA isolate from a patient hospitalized in the northeastern region of Slovenia, a national collection of 395 community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA) isolates from 2006 to 2013 was screened. An additional six mecC MRSA strains were found and characterized as spa types t843, t9397 and t10009, and multilocus sequence type ST130. The low oxacillin minimum inhibitory concentrations and absence of the mecA gene make recognition of these MRSA strains problematical for diagnostic laboratories. In such strains the presence of mecC should be determined.
    Epidemiology and infection. 07/2014;
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    ABSTRACT: Glycopeptides are known to select for heterogeneous vancomycin-intermediate Staphylococcus aureus (h-VISA) from a susceptible strain. In certain clinical situations, h-VISA strains have been isolated from patients without previous exposure to glycopeptides, such as cystic fibrosis patients who frequently receive repeated treatments with beta-lactam antibiotics. Our objective was to determine whether prolonged exposure to beta-lactam antibiotics could induce h-VISA. We exposed 3 clinical vancomycin-susceptible methicillin-resistant Staphylococcus aureus strains to ceftazidime, ceftriaxone, imipenem and to vancomycin (as a control) at sub-inhibitory concentrations for 18 days in vitro. Population analyses showed a progressive increase in vancomycin resistance; seven of the 12 derived strains obtained after induction were classified as h-VISA according to the following criteria: AUC(day 18):AUC(Mu3) ≥ 90% and/or growth on BHI agar with vancomycin 4 mg/L. The derived isolates had a thickened cell-wall proportional to the level of glycopeptide resistance. Genes known to be associated with glycopeptide resistance (vraSR, yvqF, SA1703, graRS, walKR, rpoB) were PCR-sequenced; no de novo mutation was observed upon beta-lactam exposure. To determine whether trfA, a gene encoding a glycopeptide resistance factor, was essential in selecting h-VISA upon beta-lactam pressure, a trfA knock-out strain was generated by allelic replacement. Indeed, beta-lactams exposure of this mutated strain showed no capacity to induce vancomycin resistance. In conclusion, these results showed that beta-lactam antibiotics at subinhibitory concentration can induce intermediate vancomycin resistance in vitro. This induction required an intact trfA locus. Our results suggest that prior use of beta-lactam antibiotics could compromise the vancomycin efficacy for MRSA infections treatment.
    Antimicrobial Agents and Chemotherapy 06/2014; · 4.57 Impact Factor
  • The Journal of Infectious Diseases 05/2014; · 5.85 Impact Factor
  • Journal of Antimicrobial Chemotherapy 04/2014; · 5.34 Impact Factor
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    ABSTRACT: The prevalence of CC398 methicillin-susceptible Staphylococcus aureus (MSSA) was unexpectedly high among bone and joint infections (BJIs) and nasal-colonizing isolates in France, with surprising geographical heterogeneity. With none of the major, most-known staphylococcal virulence genes, MSSA CC398 BJI was associated with reduced inflammatory syndrome and lower treatment failure rates. This article is protected by copyright. All rights reserved.
    Clinical Microbiology and Infection 03/2014; · 4.58 Impact Factor
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    ABSTRACT: Background. An outbreak of PVL-positive MSSA skin and soft tissue-infections (SSTIs) was suspected in May 2010 when recurrent SSTI was diagnosed in an inmate of a large prison in Nantes, France. Methods and findings. Retrospective and prospective investigations were performed. Microbiological characterisation was by DNA microarray testing (S. aureus genotyping - Identibac, Alere). We identified 14 inmates meeting our clinical and microbiological case definition for PVL-MSSA SSTI between March 2010 and April 2011. The SSTIs developed in tattooed areas in 4 patients and in areas shaved daily with a mechanical razor in 4 other patients. All case isolates exhibited a similar SmaI pulsed-field gel electrophoresis pattern. Microarray analysis showed that all 14 isolates harboured genes encoding PVL and enterotoxins (A, H, K, and Q) and belonged to clonal complex 1 (CC1). Individual and collective hygiene measures, education delivered to inmates and prison employees, and antibiotic treatment of SSTIs were successful in controlling the outbreak. No new cases were identified after April 2011. Routine screening for PVL-positive MSSA carriage was not feasible. Conclusions. Our data suggest that tattooing and shaving with mechanical razors may constitute risk factors for SSTIs among previously colonised inmates and contribute to the PVL-MSSA outbreak in the prison. Allowing inmates access to professional tattooists and to the hygiene and safety conditions available to people in the community would help to prevent tattoo-related infections.
    PLoS currents. 01/2014; 6.
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    ABSTRACT: Community-acquired Staphylococcus aureus necrotizing pneumonia is a life-threatening disease. Panton Valentine Leukocidin (PVL) has been associated with necrotizing pneumonia. PVL triggers inflammasome activation in human macrophages leading to IL-1β release. IL-1β activates lung epithelial cells to release IL-8. This study aimed to assess the relevance of this inflammatory cascade in vivo and to test the potential of an IL-1 receptor antagonist (IL-1Ra/Kineret) to decrease inflammation-mediated lung injury.
    PLoS ONE 01/2014; 9(6):e97546. · 3.53 Impact Factor
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    ABSTRACT: Descriptions of the epidemiology of methicillin-resistant Staphylococcus aureus (MRSA) have seldom been produced in the Caribbean, which is a major tourism destination. Using DNA microarrays and spa typing, we characterized 85 MRSA isolates from human skin and soft-tissue infections from five different islands. In the French West Indies (n = 72), the most frequently isolated clones were the same clones that are specifically isolated from mainland France [Lyon (n = 35) and Geraldine (n = 11) clones], whereas the clones that were most frequently isolated from the other islands (n = 13) corresponded with clones that have a worldwide endemic spread [Vienna/Hungarian/Brazilian (n = 5), Panton Valentine leukocidin-positive USA300 (n = 4), New York/Japan (n = 2), and pediatric (n = 1) clones]. The distribution of the major MRSA clones in the French (Guadeloupe and Martinique) and non-French West Indies (Jamaica, Trinidad, and Tobago) is different, and the clones most closely resemble those found in the home countries of the travelers who visit the islands most frequently. The distribution might be affected by tourist migration, which is specific to each island.
    Journal of Travel Medicine 09/2013; 20(5):283-8. · 1.68 Impact Factor
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    ABSTRACT: Necrotizing pneumonia attributed to Panton-Valentine leukocidin-positive Staphylococcus aureus has mainly been reported in otherwise healthy children and young adults, with a high mortality rate. Erythroderma, airway bleeding, and leukopenia have been shown to be predictive of mortality. The objectives of this study were to define the characteristics of patients with severe leukopenia at 48-h hospitalization and to update our data regarding mortality predicting factors in a larger population than we had previously described. It was designed as a case-case study nested in a cohort study. A total of 148 cases of community-acquired, necrotizing pneumonia were included. The following data were collected: basic demographic information, medical history, signs and symptoms, radiological findings and laboratory results during the first 48 h of hospitalization. The study population was divided into 2 groups: (1) with severe leukopenia (leukocyte count <=3,000 leukocytes/mL, n=62) and (2) without severe leukopenia (>3,000 leukocytes/mL, n=86). Median age was 22 years, and the male-to-female gender ratio was 1.5. The overall in-hospital mortality rate was 41.2%. Death occurred in 75.8% of severe leukopenia cases with median survival time of 4 days, and in 16.3% of cases with leukocyte count >3,000/mL (P<0.001). Multivariate analysis indicated that the factors associated with severe leukopenia were influenza-like illness (adjusted odds ratio (aOR) 4.45, 95% CI (95% confidence interval) 1.67-11.88, P=0.003), airway bleeding (aOR 4.53, 95% CI 1.85-11.13, P=0.001) and age over 30 years (aOR 2.69, 95% CI 1.08-6.68, P=0.033). A personal history of furuncles appeared to be protective (OR 0.11, 95% CI 0.01-0.96, P=0.046). S. aureus-necrotizing pneumonia is still an extremely severe disease in patients with severe leukopenia. Some factors could distinguish these patients, allowing better initial identification to initiate adapted, rapid administration of appropriate therapy.
    BMC Infectious Diseases 08/2013; 13(1):359. · 3.03 Impact Factor
  • Journal of Antimicrobial Chemotherapy 07/2013; · 5.34 Impact Factor
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    ABSTRACT: OBJECTIVES: To examine the effect of subinhibitory concentrations (sub-MICs) of antistaphylococcal drugs on Panton-Valentine leucocidin (PVL), α-haemolysin (Hla) and protein A (SpA) expression by community-acquired methicillin-resistant Staphylococcus aureus (CA-MRSA). METHODS: Five clinical isolates representing the main worldwide CA-MRSA clones were grown with sub-MICs (1/8, 1/4 and 1/2 MIC) of five antibiotics (clindamycin, daptomycin, linezolid, tigecycline and vancomycin). After 4 and 6 h of incubation, culture pellets were used for relative quantitative RT-PCR with primers specific for pvl, hla, spa and gyrB. The PVL, Hla and SpA concentrations were measured in the supernatant (for PVL and Hla) and in the cell pellet (for SpA) using specific ELISAs. RESULTS: For all strains tested, clindamycin and linezolid dramatically reduced mRNA levels of PVL and SpA. Tigecycline also decreased the PVL and SpA mRNA levels of 3/5 and 4/5 strains tested, respectively, whereas daptomycin and vancomycin had no significant effect. PVL and SpA quantification confirmed the concentration-dependent inhibition of PVL and SpA production by clindamycin and, to a lesser extent, by linezolid and tigecycline. Only clindamycin decreased Hla mRNA expression, whereas linezolid, tigecycline and daptomycin showed heterogeneous strain-dependent results, and vancomycin had no significant effect. Analysis of the Hla level revealed a stronger concentration-dependent inhibition of Hla release by clindamycin than by linezolid. CONCLUSIONS: The effect of sub-MICs on virulence expression depended on the antibiotic and the virulence factor. Clindamycin and linezolid consistently suppressed the expression of different virulence factors by CA-MRSA, whereas tigecycline specifically suppressed PVL expression. Daptomycin and vancomycin seem to have no significant effects at these concentrations.
    Journal of Antimicrobial Chemotherapy 03/2013; · 5.34 Impact Factor
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    ABSTRACT: BACKGROUND:: Staphylococcal scalded skin syndrome and toxic shock syndrome are associated with exfoliatins and superantigens, respectively; and are easy to distinguish in their usual presentation. However, there is confusion about the mild forms of these two staphylococcal diseases. These mild forms are both designated as "staphylococcal scarlet fever" despite differences in their pathophysiology and clinical presentation.Our study aimed to distinguish between the clinical characteristics of the rash associated with exfoliatins and the rash associated with superantigens. METHODS:: Patients were selected from the French National Reference Center for Staphylococci. We retrospectively compared the clinical characteristics of patients with a generalized rash during S. aureus infection. Patients that met the criteria of staphylococcal scalded skin syndrome or toxic shock syndrome were excluded. The patients were classified into two groups, depending on the presence of a gene coding for exfoliatin or for superantigenic toxin. RESULTS:: We included 13 cases with exfoliatin and 9 with superantigens. The patients of the exfoliatin group were more likely to have facial involvement, fold involvement and a superficial focus of infection. In the second group, S. aureus was isolated from a deeper focus in 8/9 patients. CONCLUSION:: Mild forms of S. aureus toxin-mediated infection affect the paediatric population. Examination made it possible to distinguish an exanthema associated with an exfoliatin from one associated with a superantigen. This early clinical distinction results in differences in management.
    The Pediatric Infectious Disease Journal 02/2013; · 3.57 Impact Factor
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    ABSTRACT: Background: To characterize the methicillin-resistant Staphylococcus aureus (MRSA) clones present in Istanbul, 102 MRSA isolates collected during a 5-year period at the Istanbul Medical Faculty Hospital were characterized using microarray analysis and phenotypic resistance profiles. Methods: Resistance to methicillin was detected with a cefoxitin disk diffusion assay and confirmed with a MRSA-agar and MRSA detection kit. Antimicrobial susceptibility testing was performed by a disk diffusion assay and interpreted according to the 2012 guidelines of the Antibiogram Committee of the French Society for Microbiology. Decreased susceptibility to glycopeptides was confirmed using the population analysis profile-area under the curve (PAP-AUC) method. The presence of the mecA gene was detected by polymerase chain reaction. Bacterial DNA was extracted according to the manufacturer's recommended protocol using commercial extraction kits. Strains were extensively characterized using the DNA microarray. Results: Isolates were grouped into six clonal complexes. The most frequently detected clone was the Vienna/Hungarian/Brazilian clone (ST239-MRSA-III), which accounted for 53.9% of the isolates. These isolates were resistant to multiple antibiotics, particularly penicillin, tetracycline, rifampicin, kanamycin, tobramycin, gentamicin, levofloxacin, erythromycin, lincomycin and fosfomycin. Furthermore, three isolates were detected by population analysis profile as heterogeneous vancomycin-intermediate S. aureus (hVISA). The UK-EMRSA-15 clone (ST22-MRSA-IV PVL negative) was detected in 9.8% of the isolates and was mainly susceptible to all anti-staphylococcal antibiotics. Seven isolates (6.9%) were positive for PVL genes and were assigned to the CC80-MRSA-IV clone (European CA-MRSA clone, three isolates), ST8-MRSA-IV clone (USA300 clone, two isolates, one ACME-positive) or ST22-MRSA-IV clone ("Regensburg EMRSA" clone, two isolates). All other clones were detected in one to six isolates and corresponded to well-known clones (e.g., Pediatric clone, Dublin EMRSA clone, WA MRSA-54/63, WA MRSA-1/57). Conclusions: This work highlighted both the high prevalence of ST239-MRSA-III clone and the large diversity of the other MRSA clones detected in a university hospital in Istanbul.
    International journal of medical sciences 01/2013; 10(12):1740-5. · 2.07 Impact Factor
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    ABSTRACT: Clonal complex 398 livestok-associated-MRSA (CC398 LA-MRSA) clone is described as a major animal pathogen that can also colonize and infect humans. CC398 methicillin susceptible Staphylococcus aureus (CC398 MSSA) is less described. We identified 126 CC398 MSSA strains of human origin within 6380 S. aureus isolates gathered between 2009 and 2011, from the French National Reference Centre for Staphylococci. They were characterized using antimicrobial susceptibility testing, spa typing, DNA microarrays (Identibac S. aureus Genotyping ®, Alere), CC398-specific sequence PCR, ermT (encoding macrolides résistance) PCR. Fifty-three CC398 LA-MRSA collected from French pigs and veal were used as comparators, and phylogenetic relations between human CC398 MSSA and animal CC398 MRSA populations were explored on the basis of spa-typing and DNA microarrays. CC398 MSSA were able to induce a large spectrum of infections (especially skin, bloodstream, and pneumonias). The prevalence rate of this clone was high in MSSA population, i.e., 24.7% in a local prospective study on nasal colonization, and 7.5% in a national prospective study on infective endocarditis. CC398 MSSA isolates were frequently (89%) erythromycin resistant, due to the presence of the ermT gene, a gene not detected in erythromycin resistant CC398 LA-MRSA strains. Expression of staphylococcal complement inhibitor (scn) and the chemotaxis inhibitory protein (chp), was also specific to this population. The CC398 MRSA signature included also a panel of antibiotic resistance genes, especially a type IV or V cassette mec and tetM. CC398 MSSA and CC398 LA-MRSA populations were closely related based on spa-typing and DNA microarrays, with the MRSA strains forming the most derived lineage in phylogenic trees. Both MSSA and MRSA populations may come from common ancestors, which would have evolved in the settings of different selective pressures, explaining the acquisition of ermT, chp and scn for MSSA, and antibiotic resistance genes for MRSA.
    PLoS ONE 01/2013; 8(11):e68462. · 3.53 Impact Factor
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    ABSTRACT: Acquisition of nasal Staphylococcus aureus (S. aureus) colonization by contaminated hands is likely an important determinant of its nasal carriage rate in health care and lab setting. The objective of our cross-sectional study was to assess the prevalence of nasal methicillin-sensitive (MSSA) or -resistant Staphylococcus aureus (MRSA) carriage among health care professionals (HCPs) attending an international symposium and to study the association between compliance with hygiene rules, individual-related parameters, and medical conditions with nasal S. aureus carriage in this population. After obtaining consent, two nasal swabs were collected. Nasal MSSA and MRSA carriage was measured by the: i) molecular approach targeting spa, mecA and mecA-orfX junction sequences, and ii) culture on selective S. aureus media combined with mecA molecular detection of isolated strains. Information on compliance with hygiene rules, demographic variables, sector of activity and long-term medication was collected by anonymous questionnaire. The participation rate was 32.3%. In total, 176 subjects from 34 countries were included in the analysis. S. aureus was isolated from the nasal swabs of 57 (32.4%) subjects, of whom 3 (5.3%) harbored MRSA strains. Overall, 123 subjects reported working in microbiology laboratories with direct manipulation of S. aureus, and 29 acknowledged regular contacts with patients. In this exposed population, hydro-alcoholic solutions appeared to have a significant protective effect against nasal S. aureus carriage (OR = 0.36; 95% CI: 0.15-0.85). Hospital work was associated with increased risk of nasal S. aureus carriage (OR = 2.38; 95% CI: 1.07-5.29). The results of this study showed that compliance with basic rules of hygiene, such as the use of hydro-alcoholic solutions, could reduce the risk of nasal S. aureus colonization. Hydro-alcoholic solution could interrupt auto-transmission of the pathogen, consequently decreasing the overall nasal carriage rate, specifically in transient carriers.
    PLoS ONE 01/2013; 8(12):e82851. · 3.53 Impact Factor
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    ABSTRACT: Epidemic community-acquired methicillin-resistant Staphylococcus aureus (CA-MRSA) is associated with more severe and acute forms of osteomyelitis than healthcare-associated (HA-) MRSA. Although S. aureus is now recognized as a facultative intracellular pathogen, the contribution of osteoblast invasion by CA-MRSA to the pathogenesis of osteomyelitis is unknown. Using an ex vivo model of intracellular infection of human osteoblasts, we demonstrated that CA-MRSA strains of diverse lineages share an enhanced ability to kill infected osteoblasts compared to HA-MRSA. Cytotoxicity comparisons of CA-MRSA isogenic deletion mutants revealed that phenol-soluble modulins (PSMs), a class of membrane-damaging exoproteins that are expressed at higher levels in CA-MRSA than in HA-MRSA, are involved in this osteoblast killing, whereas other major CA-MRSA virulence determinants, the Panton-Valentine leukocidin and alpha-toxin, are not involved. Similarly, functional agr and sarA regulators, which control the expression of PSMs and alpha-toxin, were required for the expression of the intracellular cytotoxic phenotype by CA-MRSA, whereas the saeRS regulator, which controls the expression of alpha-toxin but not PSMs, had no impact on cytotoxicity. Finally, PSM transcript levels determined by quantitative reverse-transcriptase PCR were significantly higher in CA-MRSA than in HA-MRSA strains and associated with cell damage in MRSA-infected osteoblasts. These findings provide new insights into the pathogenesis of severe CA-MRSA osteomyelitis and unravel a novel virulence strategy of CA-MRSA, based on the invasion and subsequent killing of osteoblasts by PSMs acting as intracellular toxins.
    PLoS ONE 01/2013; 8(5):e63176. · 3.53 Impact Factor
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    ABSTRACT: Clin Microbiol Infect ABSTRACT: Epidemiological data on staphylococcal scalded skin syndromes (SSSS), including bullous impetigo (BI) and generalized exfoliative syndrome (GES), are scarce. To better characterize SSSS and associated Staphylococcus aureus strains, we conducted a retrospective study of 349 cases collected in France between 1997 and 2007 by the National Reference Centre of Staphylococci. Our results showed a stationary evolution of SSSS cases, with a heterogeneous distribution of cases in France. Although notification was not exhaustive, we estimated an incidence of 0.56 cases/year/million inhabitants, in accordance with previous studies conducted in France and Europe, with a median age of 2 years old and sex ratios of 1. A seasonal effect was observed, with a higher GES/BI ratio in autumn compared with other seasons, which could be explained by the impact of viral co-infection. Genetic analysis of S. aureus strains showed that accessory gene regulator (agr) 4, exfoliative toxin A (eta) and B (etb) genes, staphylococcal and enterotoxin-like O (selo) gene and agr4 etb selo profiles were predominantly associated with GES, whereas agr2 eta and agr4 eta selo were more frequently observed with BI. Only one methicillin-resistant strain was found. Protein A (spa) typing identified two main genotypes: spa clonal complex (CC) 159/sequence-type (ST) 121 (75%) and spaCC346/ST15 (18%). spaCC159 was mainly associated with agr4 eta etb selo, agr4 eta selo and agr4 etb selo, and spaCC346 was mainly associated with agr2 eta, suggesting that French SSSS cases are caused by these two main lineages. However, in a multivariate analysis, only etb was independently associated with GES.
    Clinical Microbiology and Infection 09/2012; · 4.58 Impact Factor
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    ABSTRACT: We describe human cases and clustered animal cases of mecA(LGA251)-positive methicillin-resistant Staphylococcus aureus in France. Our report confirms that this new variant has a large distribution in Europe. It may represent a public health threat because phenotypic and genotypic tests seem unable to detect this new resistance mechanism.
    Emerging Infectious Diseases 09/2012; 18(9):1465-7. · 6.79 Impact Factor
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    ABSTRACT: Clin Microbiol Infect ABSTRACT: Staphylococcal necrotizing pneumonia (NP) is a severe disease associated with Panton-Valentine leucocidin (PVL). NP was initially described for methicillin-susceptible Staphylococcus aureus (MSSA) infection, but cases associated with methicillin-resistant S. aureus (MRSA) infection have increased concomitantly with the incidence of community-acquired MRSA worldwide. The role of methicillin resistance in the severity of NP remains controversial. The characteristics and outcomes of 133 patients with PVL-positive S. aureus community-acquired pneumonia (CAP) were compared according to methicillin resistance. Data from patients hospitalized for PVL-positive S. aureus CAP in France from 1986 to 2010 were reported to the National Reference Centre for Staphylococci and were included in the study. The primary end point was mortality. Multivariate logistic modelling and the Cox regression were used for subsequent analyses. We analysed 29 cases of PVL-MRSA and 104 cases of PVL-MSSA pneumonia. Airway haemorrhages were more frequently associated with PVL-MSSA pneumonia. However, no differences in the initial severity or the management were found between these two types of pneumonia. The rate of lethality was 39% regardless of methicillin resistance. By Cox regression analysis, methicillin resistance was not found to be a significant independent predictor of mortality at 7 or 30 days (p 0.65 and p 0.71, respectively). Our study demonstrates that methicillin resistance is not associated with the severity of staphylococcal necrotizing pneumonia.
    Clinical Microbiology and Infection 09/2012; · 4.58 Impact Factor

Publication Stats

7k Citations
596.31 Total Impact Points

Institutions

  • 2014
    • Ecole normale supérieure de Lyon
      Lyons, Rhône-Alpes, France
  • 2007–2014
    • Hospices Civils de Lyon
      Lyons, Rhône-Alpes, France
    • University of Lyon
      Lyons, Rhône-Alpes, France
    • Hospital de clinicas caracas
      Caracas, Distrito Federal, Venezuela
    • CHU de Lyon - Hôpital Gériatrique Antoine Charial 
      Lyons, Rhône-Alpes, France
  • 1999–2014
    • Claude Bernard University Lyon 1
      • • Laboratoire de biométrie et biologie evolutive (LBBE)
      • • Faculté de médecine
      Villeurbanne, Rhône-Alpes, France
  • 1993–2012
    • CHU de Lyon - Groupement Hospitalier Edouard Herriot
      Lyons, Rhône-Alpes, France
  • 2011
    • University of Gothenburg
      • Department of Infectious Diseases
      Göteborg, Vaestra Goetaland, Sweden
    • University of Texas Health Science Center at Houston
      • Center for Infectious Diseases
      Houston, Texas, United States
    • Agence Régionale de Santé (ARS)
      Lutetia Parisorum, Île-de-France, France
    • Assistance Publique – Hôpitaux de Paris
      Lutetia Parisorum, Île-de-France, France
  • 2006–2011
    • Centre Hospitalier Intercommunal Fréjus Saint-Raphael
      Saint-Raphaël, Provence-Alpes-Côte d'Azur, France
    • University of Bath
      Bath, England, United Kingdom
  • 2005–2011
    • Unité Inserm U1077
      Caen, Lower Normandy, France
  • 2010
    • French Institute of Health and Medical Research
      Lutetia Parisorum, Île-de-France, France
    • Hospital de Basurto
      Bilbo, Basque Country, Spain
  • 1996
    • Palacký University of Olomouc
      • Department of Microbiology
      Olomouc, Olomoucky kraj, Czech Republic
  • 1994–1996
    • Cancer Research Center of Lyon
      Lyons, Rhône-Alpes, France
  • 1992
    • Complutense University of Madrid
      • Facultad de Veterinaria
      Madrid, Madrid, Spain
    • University of Strasbourg
      • Institut de Bactériologie
      Strasbourg, Alsace, France
  • 1990–1992
    • Institut Pasteur
      Lutetia Parisorum, Île-de-France, France