Effects of universal versus targeted chlorhexidine skin decolonisation on the clinical and molecular epidemiology of Staphylococcus epidermidis bloodstream infections in intensive care: a controlled time-series and longitudinal genomic study

Ijeoma Nnenna Okoliegbe; Sara Aly Abdelfatah Sharaf; Susanth Alapati; Deon Roos; Antonio Ribeiro; Istifanus Nkene; Daniele Ghezzi; Stuart Reid; Victoria Austin; Dolapo Ayansina; Rebecca Wilson; Tanzeel Ur-Rehman; Benjamin J Parcell; Ian Mellor; Charis A. Marwick; Marco Oggioni; Karolin Hijazi

doi:10.2139/ssrn.4910337

Effects of universal versus targeted chlorhexidine skin decolonisation on the clinical and molecular epidemiology of Staphylococcus epidermidis bloodstream infections in intensive care: a controlled time-series and longitudinal genomic study

Ijeoma Nnenna Okoliegbe
, Sara Aly Abdelfatah Sharaf
, Susanth Alapati
, Deon Roos
, Antonio Ribeiro
, Istifanus Nkene
, Daniele Ghezzi
, Stuart Reid
, Victoria Austin
, Dolapo Ayansina
, Rebecca Wilson
, Tanzeel Ur-Rehman
, Benjamin J Parcell
, Ian Mellor
, Charis A. Marwick
, Marco Oggioni
, Karolin Hijazi^* (Corresponding Author)

^*Corresponding author for this work

Research output: Working paper › Preprint

Abstract

Background: There are concerns that chlorhexidine skin decolonisation may select multidrug resistant pathogens. We evaluated the effects of de-escalating from universal to targeted chlorhexidine decolonisation on Staphylococcus epidermidis bloodstream infections (SE-BSI).

Methods: We did a retrospective before-after control-impact time-series analysis and longitudinal genotypic study in two ICUs in Scotland. Participants were adults ≥16 years admitted between Jul 1, 2009, and Feb 28, 2022. In ICU1 (intervention site) universal decolonisation in all admissions was de-escalated to targeted decolonisation of high-risk MRSA carriers on Feb 1, 2019, while in ICU2 (control site) targeted decolonisation was applied throughout. We used multilocus sequence typing to identify sequence types (ST) from SE-BSI episodes. Whole genome sequencing was applied to a random sample from ICU1. The primary outcomes were i) all BSI incidence density, ii) MRSE incidence density, iii) probability that SE-BSI were meticillin-resistant. The effects of de-escalation on MRSE in ICU1 were estimated by differences between the intervention and control sites, before and after de-escalation.

Findings: There was no increase in all BSI incidence coinciding with de-escalation in ICU1. MRSE incidence during universal decolonisation increased more rapidly in ICU1 [2·3 (95% credible interval 1·4-3·5) and 10·9 (CI 7·2-15·4) MRSE cases per 1000 OBDs at the beginning of the study and immediately before de-escalation], compared to ICU2 [1·3 (CI 0·6-2·4) and 5·3 (CI 2·9-8·7) MRSE cases per 1000 OBDs]. De-escalation was associated with reduced MRSE due to epidemic multidrug resistant sequence types, increased susceptibility to chlorhexidine and reduced carriage of mobile genetic elements and genes for multidrug resistance and biofilm production.

Interpretation: In low MRSA incidence settings, de-escalation from universal to targeted chlorhexidine decolonisation may reduce selection of multidrug resistant S. epidermidis. ICU decolonisation practices should balance risks and benefits of biocide use and be informed by surveillance of sentinel infections.

Original language	English
Publisher	SSRN
Number of pages	36
DOIs	https://doi.org/10.2139/ssrn.4910337
Publication status	Published - 13 Aug 2024

Publication series

Name	SSRN Preprints with The Lancet
ISSN (Electronic)	1556-5068

Bibliographical note

Ackowledgements
We are indebted to Professor Ian M Gould for his critical input and invaluable expertise throughout the study. We thank the administrative and laboratory staff of the NHS Grampian and Tayside Medical Microbiology laboratories for assistance with isolate collection and anonymisation. We thank Dr Hadeel Abbood for assistance with review of existing literature and evidence. We thank Dr Elaina Collie-Duguid and the Aberdeen Centre of Genome-Enabled Biology and Medicine for their critical input and contribution to quality assurance of the genome data. This study was funded by the National Health Service Grampian Charity (grant numbers EA2771, EA2119 and EA9125).

Data Sharing
The genome data of the newly sequenced isolates for this study will be available via NCBI GenBank with publication of this Article (Bioproject unique identifier PRJNA982045). Isolate metadata has been included in the Supplementary Table 2 of this Article. R codes will be available on publication at https://github.com/DeonRoos/002---AntiRes. Requests for anonymised datasets can be made by contacting the corresponding author.

Funding

This study was funded by the National Health Service Grampian Charity (grant numbers EA2771, EA2119 and EA9125).

Funders	Funder number
National Health Service Grampian Charities	EA2771, EA2119, EA9125

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Okoliegbe, I. N., Sharaf, S. A. A., Alapati, S., Roos, D., Ribeiro, A., Nkene, I., Ghezzi, D., Reid, S., Austin, V., Ayansina, D., Wilson, R., Ur-Rehman, T., Parcell, B. J., Mellor, I., Marwick, C. A., Oggioni, M., & Hijazi, K. (2024). Effects of universal versus targeted chlorhexidine skin decolonisation on the clinical and molecular epidemiology of Staphylococcus epidermidis bloodstream infections in intensive care: a controlled time-series and longitudinal genomic study. (SSRN Preprints with The Lancet). SSRN. https://doi.org/10.2139/ssrn.4910337

Effects of universal versus targeted chlorhexidine skin decolonisation on the clinical and molecular epidemiology of Staphylococcus epidermidis bloodstream infections in intensive care: a controlled time-series and longitudinal genomic study. / Okoliegbe, Ijeoma Nnenna; Sharaf, Sara Aly Abdelfatah; Alapati, Susanth et al.
SSRN, 2024. (SSRN Preprints with The Lancet).

Research output: Working paper › Preprint

Okoliegbe, IN, Sharaf, SAA, Alapati, S, Roos, D , Ribeiro, A, Nkene, I, Ghezzi, D, Reid, S, Austin, V, Ayansina, D, Wilson, R, Ur-Rehman, T, Parcell, BJ, Mellor, I, Marwick, CA, Oggioni, M & Hijazi, K 2024 'Effects of universal versus targeted chlorhexidine skin decolonisation on the clinical and molecular epidemiology of Staphylococcus epidermidis bloodstream infections in intensive care: a controlled time-series and longitudinal genomic study' SSRN Preprints with The Lancet, SSRN. https://doi.org/10.2139/ssrn.4910337

Okoliegbe IN, Sharaf SAA, Alapati S, Roos D , Ribeiro A, Nkene I et al. Effects of universal versus targeted chlorhexidine skin decolonisation on the clinical and molecular epidemiology of Staphylococcus epidermidis bloodstream infections in intensive care: a controlled time-series and longitudinal genomic study. SSRN. 2024 Aug 13. (SSRN Preprints with The Lancet). doi: 10.2139/ssrn.4910337

Okoliegbe, Ijeoma Nnenna ; Sharaf, Sara Aly Abdelfatah ; Alapati, Susanth et al. / Effects of universal versus targeted chlorhexidine skin decolonisation on the clinical and molecular epidemiology of Staphylococcus epidermidis bloodstream infections in intensive care : a controlled time-series and longitudinal genomic study. SSRN, 2024. (SSRN Preprints with The Lancet).

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abstract = "Background: There are concerns that chlorhexidine skin decolonisation may select multidrug resistant pathogens. We evaluated the effects of de-escalating from universal to targeted chlorhexidine decolonisation on Staphylococcus epidermidis bloodstream infections (SE-BSI). Methods: We did a retrospective before-after control-impact time-series analysis and longitudinal genotypic study in two ICUs in Scotland. Participants were adults ≥16 years admitted between Jul 1, 2009, and Feb 28, 2022. In ICU1 (intervention site) universal decolonisation in all admissions was de-escalated to targeted decolonisation of high-risk MRSA carriers on Feb 1, 2019, while in ICU2 (control site) targeted decolonisation was applied throughout. We used multilocus sequence typing to identify sequence types (ST) from SE-BSI episodes. Whole genome sequencing was applied to a random sample from ICU1. The primary outcomes were i) all BSI incidence density, ii) MRSE incidence density, iii) probability that SE-BSI were meticillin-resistant. The effects of de-escalation on MRSE in ICU1 were estimated by differences between the intervention and control sites, before and after de-escalation. Findings: There was no increase in all BSI incidence coinciding with de-escalation in ICU1. MRSE incidence during universal decolonisation increased more rapidly in ICU1 [2·3 (95\% credible interval 1·4-3·5) and 10·9 (CI 7·2-15·4) MRSE cases per 1000 OBDs at the beginning of the study and immediately before de-escalation], compared to ICU2 [1·3 (CI 0·6-2·4) and 5·3 (CI 2·9-8·7) MRSE cases per 1000 OBDs]. De-escalation was associated with reduced MRSE due to epidemic multidrug resistant sequence types, increased susceptibility to chlorhexidine and reduced carriage of mobile genetic elements and genes for multidrug resistance and biofilm production. Interpretation: In low MRSA incidence settings, de-escalation from universal to targeted chlorhexidine decolonisation may reduce selection of multidrug resistant S. epidermidis. ICU decolonisation practices should balance risks and benefits of biocide use and be informed by surveillance of sentinel infections. ",

author = "Okoliegbe, \{Ijeoma Nnenna\} and Sharaf, \{Sara Aly Abdelfatah\} and Susanth Alapati and Deon Roos and Antonio Ribeiro and Istifanus Nkene and Daniele Ghezzi and Stuart Reid and Victoria Austin and Dolapo Ayansina and Rebecca Wilson and Tanzeel Ur-Rehman and Parcell, \{Benjamin J\} and Ian Mellor and Marwick, \{Charis A.\} and Marco Oggioni and Karolin Hijazi",

note = "Ackowledgements We are indebted to Professor Ian M Gould for his critical input and invaluable expertise throughout the study. We thank the administrative and laboratory staff of the NHS Grampian and Tayside Medical Microbiology laboratories for assistance with isolate collection and anonymisation. We thank Dr Hadeel Abbood for assistance with review of existing literature and evidence. We thank Dr Elaina Collie-Duguid and the Aberdeen Centre of Genome-Enabled Biology and Medicine for their critical input and contribution to quality assurance of the genome data. This study was funded by the National Health Service Grampian Charity (grant numbers EA2771, EA2119 and EA9125). Data Sharing The genome data of the newly sequenced isolates for this study will be available via NCBI GenBank with publication of this Article (Bioproject unique identifier PRJNA982045). Isolate metadata has been included in the Supplementary Table 2 of this Article. R codes will be available on publication at https://github.com/DeonRoos/002---AntiRes. Requests for anonymised datasets can be made by contacting the corresponding author. ",

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T1 - Effects of universal versus targeted chlorhexidine skin decolonisation on the clinical and molecular epidemiology of Staphylococcus epidermidis bloodstream infections in intensive care

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AU - Okoliegbe, Ijeoma Nnenna

AU - Sharaf, Sara Aly Abdelfatah

AU - Alapati, Susanth

AU - Roos, Deon

AU - Ribeiro, Antonio

AU - Nkene, Istifanus

AU - Ghezzi, Daniele

AU - Reid, Stuart

AU - Austin, Victoria

AU - Ayansina, Dolapo

AU - Wilson, Rebecca

AU - Ur-Rehman, Tanzeel

AU - Parcell, Benjamin J

AU - Mellor, Ian

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AU - Oggioni, Marco

AU - Hijazi, Karolin

N1 - Ackowledgements We are indebted to Professor Ian M Gould for his critical input and invaluable expertise throughout the study. We thank the administrative and laboratory staff of the NHS Grampian and Tayside Medical Microbiology laboratories for assistance with isolate collection and anonymisation. We thank Dr Hadeel Abbood for assistance with review of existing literature and evidence. We thank Dr Elaina Collie-Duguid and the Aberdeen Centre of Genome-Enabled Biology and Medicine for their critical input and contribution to quality assurance of the genome data. This study was funded by the National Health Service Grampian Charity (grant numbers EA2771, EA2119 and EA9125). Data Sharing The genome data of the newly sequenced isolates for this study will be available via NCBI GenBank with publication of this Article (Bioproject unique identifier PRJNA982045). Isolate metadata has been included in the Supplementary Table 2 of this Article. R codes will be available on publication at https://github.com/DeonRoos/002---AntiRes. Requests for anonymised datasets can be made by contacting the corresponding author.

PY - 2024/8/13

Y1 - 2024/8/13

N2 - Background: There are concerns that chlorhexidine skin decolonisation may select multidrug resistant pathogens. We evaluated the effects of de-escalating from universal to targeted chlorhexidine decolonisation on Staphylococcus epidermidis bloodstream infections (SE-BSI). Methods: We did a retrospective before-after control-impact time-series analysis and longitudinal genotypic study in two ICUs in Scotland. Participants were adults ≥16 years admitted between Jul 1, 2009, and Feb 28, 2022. In ICU1 (intervention site) universal decolonisation in all admissions was de-escalated to targeted decolonisation of high-risk MRSA carriers on Feb 1, 2019, while in ICU2 (control site) targeted decolonisation was applied throughout. We used multilocus sequence typing to identify sequence types (ST) from SE-BSI episodes. Whole genome sequencing was applied to a random sample from ICU1. The primary outcomes were i) all BSI incidence density, ii) MRSE incidence density, iii) probability that SE-BSI were meticillin-resistant. The effects of de-escalation on MRSE in ICU1 were estimated by differences between the intervention and control sites, before and after de-escalation. Findings: There was no increase in all BSI incidence coinciding with de-escalation in ICU1. MRSE incidence during universal decolonisation increased more rapidly in ICU1 [2·3 (95% credible interval 1·4-3·5) and 10·9 (CI 7·2-15·4) MRSE cases per 1000 OBDs at the beginning of the study and immediately before de-escalation], compared to ICU2 [1·3 (CI 0·6-2·4) and 5·3 (CI 2·9-8·7) MRSE cases per 1000 OBDs]. De-escalation was associated with reduced MRSE due to epidemic multidrug resistant sequence types, increased susceptibility to chlorhexidine and reduced carriage of mobile genetic elements and genes for multidrug resistance and biofilm production. Interpretation: In low MRSA incidence settings, de-escalation from universal to targeted chlorhexidine decolonisation may reduce selection of multidrug resistant S. epidermidis. ICU decolonisation practices should balance risks and benefits of biocide use and be informed by surveillance of sentinel infections.

AB - Background: There are concerns that chlorhexidine skin decolonisation may select multidrug resistant pathogens. We evaluated the effects of de-escalating from universal to targeted chlorhexidine decolonisation on Staphylococcus epidermidis bloodstream infections (SE-BSI). Methods: We did a retrospective before-after control-impact time-series analysis and longitudinal genotypic study in two ICUs in Scotland. Participants were adults ≥16 years admitted between Jul 1, 2009, and Feb 28, 2022. In ICU1 (intervention site) universal decolonisation in all admissions was de-escalated to targeted decolonisation of high-risk MRSA carriers on Feb 1, 2019, while in ICU2 (control site) targeted decolonisation was applied throughout. We used multilocus sequence typing to identify sequence types (ST) from SE-BSI episodes. Whole genome sequencing was applied to a random sample from ICU1. The primary outcomes were i) all BSI incidence density, ii) MRSE incidence density, iii) probability that SE-BSI were meticillin-resistant. The effects of de-escalation on MRSE in ICU1 were estimated by differences between the intervention and control sites, before and after de-escalation. Findings: There was no increase in all BSI incidence coinciding with de-escalation in ICU1. MRSE incidence during universal decolonisation increased more rapidly in ICU1 [2·3 (95% credible interval 1·4-3·5) and 10·9 (CI 7·2-15·4) MRSE cases per 1000 OBDs at the beginning of the study and immediately before de-escalation], compared to ICU2 [1·3 (CI 0·6-2·4) and 5·3 (CI 2·9-8·7) MRSE cases per 1000 OBDs]. De-escalation was associated with reduced MRSE due to epidemic multidrug resistant sequence types, increased susceptibility to chlorhexidine and reduced carriage of mobile genetic elements and genes for multidrug resistance and biofilm production. Interpretation: In low MRSA incidence settings, de-escalation from universal to targeted chlorhexidine decolonisation may reduce selection of multidrug resistant S. epidermidis. ICU decolonisation practices should balance risks and benefits of biocide use and be informed by surveillance of sentinel infections.

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DO - 10.2139/ssrn.4910337

M3 - Preprint

T3 - SSRN Preprints with The Lancet

BT - Effects of universal versus targeted chlorhexidine skin decolonisation on the clinical and molecular epidemiology of Staphylococcus epidermidis bloodstream infections in intensive care

PB - SSRN

ER -

Effects of universal versus targeted chlorhexidine skin decolonisation on the clinical and molecular epidemiology of Staphylococcus epidermidis bloodstream infections in intensive care: a controlled time-series and longitudinal genomic study

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