Routes of transmission of VIM-positive Pseudomonas aeruginosa in the adult intensive care unit-analysis of 9 years of surveillance at a university hospital using a mathematical model

Thi Mui Pham; Andrea C Büchler; Anne F Voor In 't Holt; Juliëtte A Severin; Martin C J Bootsma; Diederik Gommers; Mirjam E Kretzschmar; Margreet C Vos

doi:10.1186/s13756-022-01095-x

Routes of transmission of VIM-positive Pseudomonas aeruginosa in the adult intensive care unit-analysis of 9 years of surveillance at a university hospital using a mathematical model

Thi Mui Pham, Andrea C Büchler, Anne F Voor In 't Holt, Juliëtte A Severin, Martin C J Bootsma, Diederik Gommers, Mirjam E Kretzschmar, Margreet C Vos

Research output: Contribution to journal › Article › Academic › peer-review

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Abstract

BACKGROUND: Hospital outbreaks of multidrug resistant Pseudomonas aeruginosa are often caused by Pseudomonas aeruginosa clones which produce metallo-β-lactamases, such as Verona Integron-encoded Metallo-β-lactamase (VIM). Although different sources have been identified, the exact transmission routes often remain unknown. However, quantifying the role of different transmission routes of VIM-PA is important for tailoring infection prevention and control measures. The aim of this study is to quantify the relative importance of different transmission routes by applying a mathematical transmission model using admission and discharge dates as well as surveillance culture data of patients.

METHODS: We analyzed VIM-PA surveillance data collected between 2010 and 2018 of two intensive-care unit (ICU) wards for adult patients of the Erasmus University Medical Center Rotterdam using a mathematical transmission model. We distinguished two transmission routes: direct cross-transmission and a persistent environmental route. Based on admission, discharge dates, and surveillance cultures, we estimated the proportion of transmissions assigned to each of the routes.

RESULTS: Our study shows that only 13.7% (95% CI 1.4%, 29%) of the transmissions that occurred in these two ICU wards were likely caused by cross-transmission, leaving the vast majority of transmissions (86.3%, 95% CI 71%, 98.6%) due to persistent environmental contamination.

CONCLUSIONS: Our results emphasize that persistent contamination of the environment may be an important driver of nosocomial transmissions of VIM-PA in ICUs. To minimize the transmission risk from the environment, potential reservoirs should be regularly and thoroughly cleaned and disinfected, or redesigned.

Original language	English
Article number	55
Pages (from-to)	55
Journal	Antimicrobial Resistance and Infection Control
Volume	11
Issue number	1
DOIs	https://doi.org/10.1186/s13756-022-01095-x
Publication status	Published - 4 Apr 2022

Bibliographical note

Funding Information:
Forschungsfonds zur Förderung exzellenter Nachwuchsforschender der Universität Basel, University of Basel, Basel, Switzerland (ACB). TMP has received support from the Innovative Medicines Initiative Joint Undertaking under grant agreement no. 115737-1 (Combatting bacterial resistance in Europe - molecules gainst Gram negative infections (COMBACTE-MAGNET)), resources of which are composed of financial contribution from the European Union Seventh Framework Programme (FP 7/2007-2013) and EFPIA companies in kind contribution. The funders had no role in data collection and analysis, decision to publish, or preparation of the manuscript. (www.imi.europa.eu).

Funding Information:
We would like to thank the infection control practitioners from the Erasmus MC, especially Inge de Goeij, for their cooperation and support.

Publisher Copyright:
© 2022, The Author(s).

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Routes of transmission of VIM-positive Pseudomonas aeruginosa in the adult intensive care unit-analysis of 9 years of surveillance at a university hospital using a mathematical modelFinal published version, 1.17 MBLicence: CC BY

Cite this

Pham, T. M., Büchler, A. C., Voor In 't Holt, A. F., Severin, J. A., Bootsma, M. C. J., Gommers, D., Kretzschmar, M. E., & Vos, M. C. (2022). Routes of transmission of VIM-positive Pseudomonas aeruginosa in the adult intensive care unit-analysis of 9 years of surveillance at a university hospital using a mathematical model. Antimicrobial Resistance and Infection Control, 11(1), 55. Article 55. https://doi.org/10.1186/s13756-022-01095-x

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title = "Routes of transmission of VIM-positive Pseudomonas aeruginosa in the adult intensive care unit-analysis of 9 years of surveillance at a university hospital using a mathematical model",

abstract = "BACKGROUND: Hospital outbreaks of multidrug resistant Pseudomonas aeruginosa are often caused by Pseudomonas aeruginosa clones which produce metallo-β-lactamases, such as Verona Integron-encoded Metallo-β-lactamase (VIM). Although different sources have been identified, the exact transmission routes often remain unknown. However, quantifying the role of different transmission routes of VIM-PA is important for tailoring infection prevention and control measures. The aim of this study is to quantify the relative importance of different transmission routes by applying a mathematical transmission model using admission and discharge dates as well as surveillance culture data of patients.METHODS: We analyzed VIM-PA surveillance data collected between 2010 and 2018 of two intensive-care unit (ICU) wards for adult patients of the Erasmus University Medical Center Rotterdam using a mathematical transmission model. We distinguished two transmission routes: direct cross-transmission and a persistent environmental route. Based on admission, discharge dates, and surveillance cultures, we estimated the proportion of transmissions assigned to each of the routes.RESULTS: Our study shows that only 13.7% (95% CI 1.4%, 29%) of the transmissions that occurred in these two ICU wards were likely caused by cross-transmission, leaving the vast majority of transmissions (86.3%, 95% CI 71%, 98.6%) due to persistent environmental contamination.CONCLUSIONS: Our results emphasize that persistent contamination of the environment may be an important driver of nosocomial transmissions of VIM-PA in ICUs. To minimize the transmission risk from the environment, potential reservoirs should be regularly and thoroughly cleaned and disinfected, or redesigned.",

author = "Pham, {Thi Mui} and B{\"u}chler, {Andrea C} and {Voor In 't Holt}, {Anne F} and Severin, {Juli{\"e}tte A} and Bootsma, {Martin C J} and Diederik Gommers and Kretzschmar, {Mirjam E} and Vos, {Margreet C}",

note = "Funding Information: Forschungsfonds zur F{\"o}rderung exzellenter Nachwuchsforschender der Universit{\"a}t Basel, University of Basel, Basel, Switzerland (ACB). TMP has received support from the Innovative Medicines Initiative Joint Undertaking under grant agreement no. 115737-1 (Combatting bacterial resistance in Europe - molecules gainst Gram negative infections (COMBACTE-MAGNET)), resources of which are composed of financial contribution from the European Union Seventh Framework Programme (FP 7/2007-2013) and EFPIA companies in kind contribution. The funders had no role in data collection and analysis, decision to publish, or preparation of the manuscript. (www.imi.europa.eu). Funding Information: We would like to thank the infection control practitioners from the Erasmus MC, especially Inge de Goeij, for their cooperation and support. Publisher Copyright: {\textcopyright} 2022, The Author(s).",

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Pham, TM, Büchler, AC , Voor In 't Holt, AF , Severin, JA, Bootsma, MCJ, Gommers, D, Kretzschmar, ME & Vos, MC 2022, 'Routes of transmission of VIM-positive Pseudomonas aeruginosa in the adult intensive care unit-analysis of 9 years of surveillance at a university hospital using a mathematical model', Antimicrobial Resistance and Infection Control, vol. 11, no. 1, 55, pp. 55. https://doi.org/10.1186/s13756-022-01095-x

Routes of transmission of VIM-positive Pseudomonas aeruginosa in the adult intensive care unit-analysis of 9 years of surveillance at a university hospital using a mathematical model. / Pham, Thi Mui; Büchler, Andrea C ; Voor In 't Holt, Anne F et al.
In: Antimicrobial Resistance and Infection Control, Vol. 11, No. 1, 55, 04.04.2022, p. 55.

Research output: Contribution to journal › Article › Academic › peer-review

TY - JOUR

T1 - Routes of transmission of VIM-positive Pseudomonas aeruginosa in the adult intensive care unit-analysis of 9 years of surveillance at a university hospital using a mathematical model

AU - Pham, Thi Mui

AU - Büchler, Andrea C

AU - Voor In 't Holt, Anne F

AU - Severin, Juliëtte A

AU - Bootsma, Martin C J

AU - Gommers, Diederik

AU - Kretzschmar, Mirjam E

AU - Vos, Margreet C

N1 - Funding Information: Forschungsfonds zur Förderung exzellenter Nachwuchsforschender der Universität Basel, University of Basel, Basel, Switzerland (ACB). TMP has received support from the Innovative Medicines Initiative Joint Undertaking under grant agreement no. 115737-1 (Combatting bacterial resistance in Europe - molecules gainst Gram negative infections (COMBACTE-MAGNET)), resources of which are composed of financial contribution from the European Union Seventh Framework Programme (FP 7/2007-2013) and EFPIA companies in kind contribution. The funders had no role in data collection and analysis, decision to publish, or preparation of the manuscript. (www.imi.europa.eu). Funding Information: We would like to thank the infection control practitioners from the Erasmus MC, especially Inge de Goeij, for their cooperation and support. Publisher Copyright: © 2022, The Author(s).

PY - 2022/4/4

Y1 - 2022/4/4

N2 - BACKGROUND: Hospital outbreaks of multidrug resistant Pseudomonas aeruginosa are often caused by Pseudomonas aeruginosa clones which produce metallo-β-lactamases, such as Verona Integron-encoded Metallo-β-lactamase (VIM). Although different sources have been identified, the exact transmission routes often remain unknown. However, quantifying the role of different transmission routes of VIM-PA is important for tailoring infection prevention and control measures. The aim of this study is to quantify the relative importance of different transmission routes by applying a mathematical transmission model using admission and discharge dates as well as surveillance culture data of patients.METHODS: We analyzed VIM-PA surveillance data collected between 2010 and 2018 of two intensive-care unit (ICU) wards for adult patients of the Erasmus University Medical Center Rotterdam using a mathematical transmission model. We distinguished two transmission routes: direct cross-transmission and a persistent environmental route. Based on admission, discharge dates, and surveillance cultures, we estimated the proportion of transmissions assigned to each of the routes.RESULTS: Our study shows that only 13.7% (95% CI 1.4%, 29%) of the transmissions that occurred in these two ICU wards were likely caused by cross-transmission, leaving the vast majority of transmissions (86.3%, 95% CI 71%, 98.6%) due to persistent environmental contamination.CONCLUSIONS: Our results emphasize that persistent contamination of the environment may be an important driver of nosocomial transmissions of VIM-PA in ICUs. To minimize the transmission risk from the environment, potential reservoirs should be regularly and thoroughly cleaned and disinfected, or redesigned.

AB - BACKGROUND: Hospital outbreaks of multidrug resistant Pseudomonas aeruginosa are often caused by Pseudomonas aeruginosa clones which produce metallo-β-lactamases, such as Verona Integron-encoded Metallo-β-lactamase (VIM). Although different sources have been identified, the exact transmission routes often remain unknown. However, quantifying the role of different transmission routes of VIM-PA is important for tailoring infection prevention and control measures. The aim of this study is to quantify the relative importance of different transmission routes by applying a mathematical transmission model using admission and discharge dates as well as surveillance culture data of patients.METHODS: We analyzed VIM-PA surveillance data collected between 2010 and 2018 of two intensive-care unit (ICU) wards for adult patients of the Erasmus University Medical Center Rotterdam using a mathematical transmission model. We distinguished two transmission routes: direct cross-transmission and a persistent environmental route. Based on admission, discharge dates, and surveillance cultures, we estimated the proportion of transmissions assigned to each of the routes.RESULTS: Our study shows that only 13.7% (95% CI 1.4%, 29%) of the transmissions that occurred in these two ICU wards were likely caused by cross-transmission, leaving the vast majority of transmissions (86.3%, 95% CI 71%, 98.6%) due to persistent environmental contamination.CONCLUSIONS: Our results emphasize that persistent contamination of the environment may be an important driver of nosocomial transmissions of VIM-PA in ICUs. To minimize the transmission risk from the environment, potential reservoirs should be regularly and thoroughly cleaned and disinfected, or redesigned.

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Pham TM, Büchler AC , Voor In 't Holt AF , Severin JA, Bootsma MCJ, Gommers D et al. Routes of transmission of VIM-positive Pseudomonas aeruginosa in the adult intensive care unit-analysis of 9 years of surveillance at a university hospital using a mathematical model. Antimicrobial Resistance and Infection Control. 2022 Apr 4;11(1):55. 55. doi: 10.1186/s13756-022-01095-x