Skip to main content
Top
Published in: Antimicrobial Resistance & Infection Control 1/2018

Open Access 01-12-2018 | Research

VIM-positive Pseudomonas aeruginosa in a large tertiary care hospital: matched case-control studies and a network analysis

Authors: Anne F. Voor in ‘t holt, Juliëtte A. Severin, Margot B. H. Hagenaars, Inge de Goeij, Diederik Gommers, Margreet C. Vos

Published in: Antimicrobial Resistance & Infection Control | Issue 1/2018

Login to get access

Abstract

Background

Emergence of multidrug-resistant Pseudomonas aeruginosa is of global concern. We aimed to identify epidemiological relationships, the most common way of transmission, and risk factors for presence of Verona Integron-encoded Metallo-β-lactamase (VIM)-positive P. aeruginosa (VIM-PA).

Methods

We conducted a network analysis and matched case-control studies (1:2:2). Controls were hospital-based and matched with cases for ward, day of admission (control group 1 and 2) and time between admission and the identification of VIM-PA (control group 1). The network was visualized using Cytoscape, and risk factors were determined using conditional logistic regression.

Results

Between August 2003 and April 2015, 144 case patients and 576 control patients were recruited. We identified 307 relationships in 114 out of these 144 patients, with most relationships (84.7%) identified at the same department < 3 months after a previous case patient was discharged. In the multivariable model, having undergone ≥1 gastroscopy (odds ratio [OR] = 4.40, 95% confidence interval [CI] = 2.00 to 9.65 and OR = 2.47; 95% CI = 1.12 to 5.49), > 10 day use of selective digestive tract decontamination (SDD) (OR = 2.97; 95% CI = 1.02 to 8.68 and OR = 4.61; 95% CI = 1.22 to 17.37), and use of quinolones (OR = 3.29; 95% CI = 1.34 to 8.10 and OR = 3.95; 95% CI = 1.13 to 13.83 and OR = 4.47; 95% CI = 1.75 to 11.43) were identified as risk factors when using both control groups.

Conclusions

The network analysis indicated that the majority of transmissions occurred on the wards, but through unidentified and presumably persistent sources, which are most likely in the innate hospital environment. Previous use of certain antibiotic regimens made patients prone to VIM-PA carriage. Additionally, gastroscopy could be considered as a high-risk procedure in patients with risk factors. Our results add to the growing body of evidence that infection control measures targeting VIM-PA should be focused on reducing antibiotics and eliminating sources in the environment.
Appendix
Available only for authorised users
Literature
1.
go back to reference Albiger B, Glasner C, Struelens MJ, Grundmann H, Monnet DL, European Survey of Carbapenemase-Producing Enterobacteriaceae working group. Carbapenemase-producing Enterobacteriaceae in Europe: assessment by national experts from 38 countries, May 2015. Euro Surveill. 2015;20:1–18. Albiger B, Glasner C, Struelens MJ, Grundmann H, Monnet DL, European Survey of Carbapenemase-Producing Enterobacteriaceae working group. Carbapenemase-producing Enterobacteriaceae in Europe: assessment by national experts from 38 countries, May 2015. Euro Surveill. 2015;20:1–18.
2.
go back to reference Hong DJ, Bae IK, Jang IH, Jeong SH, Kang HK, Lee K. Epidemiology and characteristics of Metallo-beta-lactamase-producing Pseudomonas aeruginosa. Infect Chemother. 2015;47:81–97.CrossRefPubMedPubMedCentral Hong DJ, Bae IK, Jang IH, Jeong SH, Kang HK, Lee K. Epidemiology and characteristics of Metallo-beta-lactamase-producing Pseudomonas aeruginosa. Infect Chemother. 2015;47:81–97.CrossRefPubMedPubMedCentral
3.
go back to reference Carmeli Y, Troillet N, Karchmer AW, Samore MH. Health and economic outcomes of antibiotic resistance in Pseudomonas aeruginosa. Arch Intern Med. 1999;159:1127–32.CrossRefPubMed Carmeli Y, Troillet N, Karchmer AW, Samore MH. Health and economic outcomes of antibiotic resistance in Pseudomonas aeruginosa. Arch Intern Med. 1999;159:1127–32.CrossRefPubMed
4.
go back to reference Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P, Hickey MJ, Brinkman FSL, Hufnagle WO, Kowalik DJ, Lagrou M, et al. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature. 2000;406:959–64.CrossRefPubMed Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P, Hickey MJ, Brinkman FSL, Hufnagle WO, Kowalik DJ, Lagrou M, et al. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature. 2000;406:959–64.CrossRefPubMed
5.
go back to reference Suarez C, Pena C, Gavalda L, Tubau F, Manzur A, Dominguez MA, Pujol M, Gudiol F, Ariza J. Influence of carbapenem resistance on mortality and the dynamics of mortality in Pseudomonas aeruginosa bloodstream infection. Int J Infect Dis. 2010;14(Suppl 3):e73–8.CrossRefPubMed Suarez C, Pena C, Gavalda L, Tubau F, Manzur A, Dominguez MA, Pujol M, Gudiol F, Ariza J. Influence of carbapenem resistance on mortality and the dynamics of mortality in Pseudomonas aeruginosa bloodstream infection. Int J Infect Dis. 2010;14(Suppl 3):e73–8.CrossRefPubMed
6.
go back to reference Zhang Y, Chen XL, Huang AW, Liu SL, Liu WJ, Zhang N, Lu XZ. Mortality attributable to carbapenem-resistant Pseudomonas aeruginosa bacteremia: a meta-analysis of cohort studies. Emerg Microbes Infect. 2016;5:e27.CrossRefPubMedPubMedCentral Zhang Y, Chen XL, Huang AW, Liu SL, Liu WJ, Zhang N, Lu XZ. Mortality attributable to carbapenem-resistant Pseudomonas aeruginosa bacteremia: a meta-analysis of cohort studies. Emerg Microbes Infect. 2016;5:e27.CrossRefPubMedPubMedCentral
8.
go back to reference Walsh TR. Emerging carbapenemases: a global perspective. Int J Antimicrob Agents. 2010;36(Suppl 3):S8–14.CrossRefPubMed Walsh TR. Emerging carbapenemases: a global perspective. Int J Antimicrob Agents. 2010;36(Suppl 3):S8–14.CrossRefPubMed
9.
go back to reference Van der Bij AK, Van der Zwan D, Peirano G, Severin JA, Pitout JD, Van Westreenen M, Goessens WH, Group M-PSS. Metallo-beta-lactamase-producing Pseudomonas aeruginosa in the Netherlands: the nationwide emergence of a single sequence type. Clin Microbiol Infect. 2012;18:E369–72.CrossRefPubMed Van der Bij AK, Van der Zwan D, Peirano G, Severin JA, Pitout JD, Van Westreenen M, Goessens WH, Group M-PSS. Metallo-beta-lactamase-producing Pseudomonas aeruginosa in the Netherlands: the nationwide emergence of a single sequence type. Clin Microbiol Infect. 2012;18:E369–72.CrossRefPubMed
10.
go back to reference Hota S, Hirji Z, Stockton K, Lemieux C, Dedier H, Wolfaardt G, Gardam MA. Outbreak of multidrug-resistant Pseudomonas aeruginosa colonization and infection secondary to imperfect intensive care unit room design. Infect Control Hosp Epidemiol. 2009;30:25–33.CrossRefPubMed Hota S, Hirji Z, Stockton K, Lemieux C, Dedier H, Wolfaardt G, Gardam MA. Outbreak of multidrug-resistant Pseudomonas aeruginosa colonization and infection secondary to imperfect intensive care unit room design. Infect Control Hosp Epidemiol. 2009;30:25–33.CrossRefPubMed
11.
go back to reference Otter JA, Vickery K, Walker JT, deLancey Pulcini E, Stoodley P, Goldenberg SD, Salkeld JA, Chewins J, Yezli S, Edgeworth JD. Surface-attached cells, biofilms and biocide susceptibility: implications for hospital cleaning and disinfection. J Hosp Infect. 2015;89:16–27.CrossRefPubMed Otter JA, Vickery K, Walker JT, deLancey Pulcini E, Stoodley P, Goldenberg SD, Salkeld JA, Chewins J, Yezli S, Edgeworth JD. Surface-attached cells, biofilms and biocide susceptibility: implications for hospital cleaning and disinfection. J Hosp Infect. 2015;89:16–27.CrossRefPubMed
12.
go back to reference Van der Bij AK, Van Mansfeld R, Peirano G, Goessens WH, Severin JA, Pitout JD, Willems R, Van Westreenen M. First outbreak of VIM-2 metallo-beta-lactamase-producing Pseudomonas aeruginosa in The Netherlands: microbiology, epidemiology and clinical outcomes. Int J Antimicrob Agents. 2011;37:513–8.CrossRefPubMed Van der Bij AK, Van Mansfeld R, Peirano G, Goessens WH, Severin JA, Pitout JD, Willems R, Van Westreenen M. First outbreak of VIM-2 metallo-beta-lactamase-producing Pseudomonas aeruginosa in The Netherlands: microbiology, epidemiology and clinical outcomes. Int J Antimicrob Agents. 2011;37:513–8.CrossRefPubMed
13.
go back to reference Voor In ‘t Holt AF, Severin JA, Lesaffre EM, Vos MC. A systematic review and meta-analyses show that carbapenem use and medical devices are the leading risk factors for carbapenem-resistant Pseudomonas aeruginosa. Antimicrob Agents Chemother. 2014;58:2626–37.CrossRefPubMedPubMedCentral Voor In ‘t Holt AF, Severin JA, Lesaffre EM, Vos MC. A systematic review and meta-analyses show that carbapenem use and medical devices are the leading risk factors for carbapenem-resistant Pseudomonas aeruginosa. Antimicrob Agents Chemother. 2014;58:2626–37.CrossRefPubMedPubMedCentral
14.
go back to reference de Smet AM, Kluytmans JA, Cooper BS, Mascini EM, Benus RF, van der Werf TS, van der Hoeven JG, Pickkers P, Bogaers-Hofman D, van der Meer NJ, et al. Decontamination of the digestive tract and oropharynx in ICU patients. N Engl J Med. 2009;360:20–31.CrossRefPubMed de Smet AM, Kluytmans JA, Cooper BS, Mascini EM, Benus RF, van der Werf TS, van der Hoeven JG, Pickkers P, Bogaers-Hofman D, van der Meer NJ, et al. Decontamination of the digestive tract and oropharynx in ICU patients. N Engl J Med. 2009;360:20–31.CrossRefPubMed
15.
go back to reference Verfaillie CJ, Bruno MJ, Voor in ‘t Holt AF, Buijs JG, Poley JW, Loeve AJ, Severin JA, Abel LF, Smit BJ, de Goeij I, Vos MC. Withdrawal of a novel-design duodenoscope ends outbreak of a VIM-2-producing Pseudomonas aeruginosa. Endoscopy. 2015;47:493–502.CrossRefPubMed Verfaillie CJ, Bruno MJ, Voor in ‘t Holt AF, Buijs JG, Poley JW, Loeve AJ, Severin JA, Abel LF, Smit BJ, de Goeij I, Vos MC. Withdrawal of a novel-design duodenoscope ends outbreak of a VIM-2-producing Pseudomonas aeruginosa. Endoscopy. 2015;47:493–502.CrossRefPubMed
16.
go back to reference Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003;13:2498–504.CrossRefPubMedPubMedCentral Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003;13:2498–504.CrossRefPubMedPubMedCentral
17.
go back to reference Knoester M, de Boer MG, Maarleveld JJ, Claas EC, Bernards AT, de Jonge E, van Dissel JT, Veldkamp KE. An integrated approach to control a prolonged outbreak of multidrug-resistant Pseudomonas aeruginosa in an intensive care unit. Clin Microbiol Infect. 2014;20:O207–15.CrossRefPubMed Knoester M, de Boer MG, Maarleveld JJ, Claas EC, Bernards AT, de Jonge E, van Dissel JT, Veldkamp KE. An integrated approach to control a prolonged outbreak of multidrug-resistant Pseudomonas aeruginosa in an intensive care unit. Clin Microbiol Infect. 2014;20:O207–15.CrossRefPubMed
18.
19.
go back to reference Muscarella LF. Risk of transmission of carbapenem-resistant Enterobacteriaceae and related “superbugs” during gastrointestinal endoscopy. World J Gastrointest Endosc. 2014;6:457–74.CrossRefPubMedPubMedCentral Muscarella LF. Risk of transmission of carbapenem-resistant Enterobacteriaceae and related “superbugs” during gastrointestinal endoscopy. World J Gastrointest Endosc. 2014;6:457–74.CrossRefPubMedPubMedCentral
20.
go back to reference von Elm E, Altman DG, Egger M, Pocock SJ, Gotzsche PC, Vandenbroucke JP, Initiative S. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. Lancet. 2007;370:1453–7.CrossRefPubMed von Elm E, Altman DG, Egger M, Pocock SJ, Gotzsche PC, Vandenbroucke JP, Initiative S. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. Lancet. 2007;370:1453–7.CrossRefPubMed
21.
go back to reference Brossier F, Micaelo M, Luyt CE, Lu Q, Chastre J, Arbelot C, Trouillet JL, Combes A, Rouby JJ, Jarlier V, Aubry A. Could the DiversiLab(R) semi-automated repetitive-sequence-based PCR be an acceptable technique for typing isolates of Pseudomonas aeruginosa? An answer from our experience and a review of the literature. Can J Microbiol. 2015;61:903–12.CrossRefPubMed Brossier F, Micaelo M, Luyt CE, Lu Q, Chastre J, Arbelot C, Trouillet JL, Combes A, Rouby JJ, Jarlier V, Aubry A. Could the DiversiLab(R) semi-automated repetitive-sequence-based PCR be an acceptable technique for typing isolates of Pseudomonas aeruginosa? An answer from our experience and a review of the literature. Can J Microbiol. 2015;61:903–12.CrossRefPubMed
Metadata
Title
VIM-positive Pseudomonas aeruginosa in a large tertiary care hospital: matched case-control studies and a network analysis
Authors
Anne F. Voor in ‘t holt
Juliëtte A. Severin
Margot B. H. Hagenaars
Inge de Goeij
Diederik Gommers
Margreet C. Vos
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Antimicrobial Resistance & Infection Control / Issue 1/2018
Electronic ISSN: 2047-2994
DOI
https://doi.org/10.1186/s13756-018-0325-1

Other articles of this Issue 1/2018

Antimicrobial Resistance & Infection Control 1/2018 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine