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Molecular epidemiology of Pseudomonas aeruginosa isolated from infected ICU patients: a French multicenter 2012–2013 study

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Abstract

Although Pseudomonas aeruginosa has a non-clonal epidemic population structure, recent studies have provided evidence of the existence of epidemic high-risk clones. The aim of this study was to assess the molecular epidemiology of P. aeruginosa isolates responsible for infections in French ICUs, regardless of resistance patterns. For a 1-year period, all non-duplicate P. aeruginosa isolated from bacteremia and pulmonary infections in ten adult ICUs of six French university hospitals were characterized by antimicrobial susceptibility testing and genotyping (MLST and PFGE). We identified β-lactamases with an extended spectrum phenotypically and by sequencing. The 104 isolates tested were distributed in 46 STs, of which 7 epidemic high-risk (EHR) clones over-represented: ST111, ST175, ST235, ST244, ST253, ST308, and ST395. Multidrug-resistant (MDR) isolates mostly clustered in these EHR clones, which frequently spread within hospitals. Only one ST233 isolate produced the carbapenemase VIM-2. PFGE analysis suggests frequent intra-hospital cross-transmission involving EHR clones. For ST395 and ST308, we also observed the progression from wild-type to MDR resistance pattern within the same PFGE pattern. Molecular epidemiology of P. aeruginosa in French ICUs is characterized by high clonal diversity notably among antimicrobial susceptible isolates and the over-representation of EHR clones, particularly within MDR isolates, even though multidrug resistance is not a constant inherent trait of EHR clones.

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Abbreviations

EHR:

epidemic high-risk

ESBL:

extended-spectrum β-lactamase

ES-OXA:

extended-spectrum oxacillinase

ICU:

intensive care unit

MBL:

metallo-β-lactamase

MDR:

multidrug resistant

MLST:

multilocus sequence typing

PFGE:

pulsed-field gel electrophoresis

PT:

pulsotype

ST:

sequence type

WT:

wild type

XDR:

extensive drug resistant

References

  1. Poole K (2011) Pseudomonas aeruginosa: resistance to the max. Front Microbiol 2:65. https://doi.org/10.3389/fmicb.2011.00065

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Oliver A, Mulet X, Lopez-Causape C, Juan C (2015) The increasing threat of Pseudomonas aeruginosa high-risk clones. Drug Resist Updat 21-22:41–59. https://doi.org/10.1016/j.drup.2015.08.002

    Article  PubMed  Google Scholar 

  3. Abdouchakour F, Aujoulat F, Licznar-Fajardo P, Marchandin H, Toubiana M, Parer S, Lotthe A, Jumas-Bilak E (2018) Intraclonal variations of resistance and phenotype in Pseudomonas aeruginosa epidemic high-risk clone ST308: a key to success within a hospital? Int J Med Microbiol 308(2):279–289. https://doi.org/10.1016/j.ijmm.2017.11.008

    Article  CAS  PubMed  Google Scholar 

  4. Cabot G, Ocampo-Sosa AA, Dominguez MA, Gago JF, Juan C, Tubau F, Rodriguez C, Moya B, Pena C, Martinez-Martinez L, Oliver A (2012) Genetic markers of widespread extensively drug-resistant Pseudomonas aeruginosa high-risk clones. Antimicrob Agents Chemother 56(12):6349–6357. https://doi.org/10.1128/AAC.01388-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Treepong P, Kos VN, Guyeux C, Blanc DS, Bertrand X, Valot B, Hocquet D (2018) Global emergence of the widespread Pseudomonas aeruginosa ST235 clone. Clin Microbiol Infect 24(3):258–266. https://doi.org/10.1016/j.cmi.2017.06.018

    Article  CAS  PubMed  Google Scholar 

  6. Hocquet D, Dehecq B, Bertrand X, Plesiat P (2011) Strain-tailored double-disk synergy test detects extended-spectrum oxacillinases in Pseudomonas aeruginosa. J Clin Microbiol 49(6):2262–2265. https://doi.org/10.1128/JCM.02585-10

    Article  PubMed  PubMed Central  Google Scholar 

  7. Hocquet D, Plesiat P, Dehecq B, Mariotte P, Talon D, Bertrand X (2010) Nationwide investigation of extended-spectrum beta-lactamases, metallo-beta-lactamases, and extended-spectrum oxacillinases produced by ceftazidime-resistant Pseudomonas aeruginosa strains in France. Antimicrob Agents Chemother 54(8):3512–3515. https://doi.org/10.1128/AAC.01646-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Curran B, Jonas D, Grundmann H, Pitt T, Dowson CG (2004) Development of a multilocus sequence typing scheme for the opportunistic pathogen Pseudomonas aeruginosa. J Clin Microbiol 42(12):5644–5649

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Cholley P, Ka R, Guyeux C, Thouverez M, Guessennd N, Ghebremedhin B, Frank T, Bertrand X, Hocquet D (2014) Population structure of clinical Pseudomonas aeruginosa from West and Central African countries. PLoS One 9(9):e107008. https://doi.org/10.1371/journal.pone.0107008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Witney AA, Gould KA, Pope CF, Bolt F, Stoker NG, Cubbon MD, Bradley CR, Fraise A, Breathnach AS, Butcher PD, Planche TD, Hinds J (2014) Genome sequencing and characterization of an extensively drug-resistant sequence type 111 serotype O12 hospital outbreak strain of Pseudomonas aeruginosa. Clin Microbiol Infect 20(10):O609–O618. https://doi.org/10.1111/1469-0691.12528

    Article  CAS  PubMed  Google Scholar 

  11. Turton JF, Wright L, Underwood A, Witney AA, Chan YT, Al-Shahib A, Arnold C, Doumith M, Patel B, Planche TD, Green J, Holliman R, Woodford N (2015) High-resolution analysis by whole-genome sequencing of an international lineage (sequence type 111) of Pseudomonas aeruginosa associated with metallo-carbapenemases in the United Kingdom. J Clin Microbiol 53(8):2622–2631. https://doi.org/10.1128/JCM.00505-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Cabot G, Lopez-Causape C, Ocampo-Sosa AA, Sommer LM, Dominguez MA, Zamorano L, Juan C, Tubau F, Rodriguez C, Moya B, Pena C, Martinez-Martinez L, Plesiat P, Oliver A (2016) Deciphering the resistome of the widespread Pseudomonas aeruginosa sequence type 175 international high-risk clone through whole-genome sequencing. Antimicrob Agents Chemother 60(12):7415–7423. https://doi.org/10.1128/AAC.01720-16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Bertrand X, Bailly P, Blasco G, Balvay P, Boillot A, Talon D (2000) Large outbreak in a surgical intensive care unit of colonization or infection with Pseudomonas aeruginosa that overexpressed an active efflux pump. Clin Infect Dis 31(4):E9–E14. https://doi.org/10.1086/318117

    Article  CAS  PubMed  Google Scholar 

  14. Gbaguidi-Haore H, Varin A, Cholley P, Thouverez M, Hocquet D, Bertrand X (2018) A bundle of measures to control an outbreak of Pseudomonas aeruginosa associated with P-trap contamination. Infect Control Hosp Epidemiol 39(2):164–169. https://doi.org/10.1017/ice.2017.304

    Article  PubMed  Google Scholar 

  15. Quick J, Cumley N, Wearn CM, Niebel M, Constantinidou C, Thomas CM, Pallen MJ, Moiemen NS, Bamford A, Oppenheim B, Loman NJ (2014) Seeking the source of Pseudomonas aeruginosa infections in a recently opened hospital: an observational study using whole-genome sequencing. BMJ Open 4(11):e006278. https://doi.org/10.1136/bmjopen-2014-006278

    Article  PubMed  PubMed Central  Google Scholar 

  16. Petitjean M, Martak D, Silvant A, Bertrand X, Valot B, Hocquet D (2017) Genomic characterization of a local epidemic Pseudomonas aeruginosa reveals specific features of the widespread clone ST395. Microb Genom 3(10):e000129. https://doi.org/10.1099/mgen.0.000129

    Article  PubMed  PubMed Central  Google Scholar 

  17. Willmann M, Bezdan D, Zapata L, Susak H, Vogel W, Schroppel K, Liese J, Weidenmaier C, Autenrieth IB, Ossowski S, Peter S (2015) Analysis of a long-term outbreak of XDR Pseudomonas aeruginosa: a molecular epidemiological study. J Antimicrob Chemother 70(5):1322–1330. https://doi.org/10.1093/jac/dku546

    Article  CAS  PubMed  Google Scholar 

  18. Papagiannitsis CC, Medvecky M, Chudejova K, Skalova A, Rotova V, Spanelova P, Jakubu V, Zemlickova H, Hrabak J (2018) Molecular characterization of carbapenemase-producing Pseudomonas aeruginosa of Czech origin and evidence for clonal spread of extensively resistant sequence type 357 expressing IMP-7 metallo-beta-lactamase. Antimicrob Agents Chemother 61(12). https://doi.org/10.1128/AAC.01811-17

  19. Fan X, Wu Y, Xiao M, Xu ZP, Kudinha T, Bazaj A, Kong F, Xu YC (2016) Diverse genetic background of multidrug-resistant Pseudomonas aeruginosa from mainland China, and emergence of an extensively drug-resistant ST292 clone in Kunming. Sci Rep 6:26522. https://doi.org/10.1038/srep26522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Nascimento AP, Ortiz MF, Martins WM, Morais GL, Fehlberg LC, Almeida LG, Ciapina LP, Gales AC, Vasconcelos AT (2016) Intraclonal genome stability of the metallo-beta-lactamase SPM-1-producing Pseudomonas aeruginosa ST277, an endemic clone disseminated in Brazilian hospitals. Front Microbiol 7:1946. https://doi.org/10.3389/fmicb.2016.01946

    Article  PubMed  PubMed Central  Google Scholar 

  21. Cabrolier N, Sauget M, Bertrand X, Hocquet D (2015) Matrix-assisted laser desorption ionization-time of flight mass spectrometry identifies Pseudomonas aeruginosa high-risk clones. J Clin Microbiol 53(4):1395–1398. https://doi.org/10.1128/JCM.00210-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We thank the ICUs (Gilles Capellier, Emmanuel Samain, Christian Auboyer, Fabrice Zéni, Christophe Mariat, Anne-Charlotte Tellier, Martine Ferandière, François Lagarrigue, Charlotte Arbelot, Corinne Vezinet), microbiology laboratories (Anne Carricajo, Florence Grattard, Julie Gagnaire, Hanaa Benmansour), and infection control teams of the six participating centers.

Financial support

This work was supported by the French Ministry of Health (PHRC national 2011).

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Authors and Affiliations

Authors

Contributions

CS participated in the design of the study, acquisition of data, coordinated the study and in the article redaction. JR, NvdMM, PB, AMR, and VD participated in the acquisition of data and in the article redaction. PC and MT carried out the bacterial typing. DH coordinated the bacteriology study and participated in the redaction. XB conceived the study, participated in the acquisition of data in its design, and wrote the article.

Corresponding author

Correspondence to Xavier Bertrand.

Ethics declarations

Approval and written informed consent from all subjects or their legally authorized representatives were obtained before study initiation. The study was approved by the ethical committee “Comité d’Etude Clinique” of the Besançon University Hospital, Besançon, France, references: 2011-A01013-38.

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The authors declare that they have no conflicts of interest.

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Slekovec, C., Robert, J., van der Mee-Marquet, N. et al. Molecular epidemiology of Pseudomonas aeruginosa isolated from infected ICU patients: a French multicenter 2012–2013 study. Eur J Clin Microbiol Infect Dis 38, 921–926 (2019). https://doi.org/10.1007/s10096-019-03519-w

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