Environmental surveillance of ESBL and carbapenemase-producing gram-negative bacteria in a Ghanaian Tertiary Hospital

Joseph Elikem Efui Acolatse; Edward A.R. Portal; Ian Boostrom; George Akafity; Mavis Puopelle Dakroah; Victoria J. Chalker; Kirsty Sands; Owen B. Spiller

doi:10.1186/s13756-022-01090-2

Environmental surveillance of ESBL and carbapenemase-producing gram-negative bacteria in a Ghanaian Tertiary Hospital

Joseph Elikem Efui Acolatse, Edward A.R. Portal, Ian Boostrom, George Akafity, Mavis Puopelle Dakroah, Victoria J. Chalker, Kirsty Sands^*, Owen B. Spiller

^*Corresponding author for this work

UK Health Security Agency

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

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Abstract

Background: The burden of antibiotic resistant infection is mainly felt in low-to-middle income countries, where the rate of antimicrobial resistance is largely under-surveyed and under huge pressure from unregulated, disparate and often self-guided access to antimicrobials. Nosocomial infections from hospital environments have been shown to be a particularly prevalent source of multi-drug resistant strains, yet surveillance of hospital environmental contamination is often not investigated.

Methods: The study was prospective, observational and cross-sectional, sampling 231 high and low touch surfaces from 15th March to 13th April 2021, from five wards in the Cape Coast Teaching Hospital, Ghana. Microbial growth in the presence of vancomycin and either meropenem or cefotaxime was examined and bacterial species were identified by MALDI-TOF. The presence of common extended-spectrum β-lactamases (ESBL) and carbapenemase antimicrobial resistance genes (ARG) were identified through PCR screening, which were confirmed by phenotypic antimicrobial susceptibility determination. Isolates positive for carbapenem resistance genes were sequenced using a multi-platform approach.

Results: We recovered microbial growth from 99% of swabs (n = 229/231) plated on agar in the absence of antimicrobials. Multiple sites were found to be colonised with resistant bacteria throughout the hospital setting. Bacteria with multi-drug resistance and ARG of concern were isolated from high and low touch points with evidence of strain dissemination throughout the environment. A total of 21 differing species of bacteria carrying ARG were isolated. The high prevalence of Acinetobacter baumannii carrying bla_NDM-1 observed was further characterised by whole genome sequencing and phylogenetic analysis to determine the relationship between resistant strains found in different wards.

Conclusion: Evidence of multiple clonal incursions of MDR bacteria of high sepsis risk were found in two separate wards for a regional hospital in Ghana. The prevalence of multiple bla_NDM carrying species in combination with combinations of ESBLs was particularly concerning and unexpected in Africa. We also identify strains carrying tet(X3), bla_VIM-5 or bla_DIM-1 showing a high diversity of carbapenamases present as a reservoir in a hospital setting. Findings of multi-drug resistant bacteria from multiple environmental sites throughout the hospital will inform future IPC practices and aid research prioritisation for AMR in Ghana.

Original language	English
Article number	49
Number of pages	15
Journal	Antimicrobial Resistance and Infection Control
Volume	11
Issue number	1
DOIs	https://doi.org/10.1186/s13756-022-01090-2
Publication status	Published - 16 Mar 2022

Bibliographical note

Funding Information: We are grateful to the Chief Executive, the Laboratory manager, and all the nurse-in-charges of the various wards sampled in the Cape Coast Teaching Hospital for their support during this study. We are thankful to Dr Maria Mendes De Carvalho for the development of the CTX-M-15 PCR and to Dr Brekhna Hassan for developing the carbapenemase multiplex PCR (data unpublished). We would like to thank the NHS staff in the Specialist Antimicrobial Chemotherapy Unit (SACU) Public Health Wales for supporting access to the MALDI-TOF MS instrument. Bioinformatics analysis was undertaken using the supercomputing facilities at Cardiff University operated by Advanced Research Computing at Cardiff (ARCCA) on behalf of the Cardiff Supercomputing Facility and the HPC Wales and Supercomputing Wales (SCW) projects. We acknowledge the support of the latter, which is part-funded by the European Regional Development Fund (ERDF) via the Welsh Government. Joseph Elikem Efui Acolatse has received support and guidance for the study/project through ESCMID's mentorship programme by Victoria J. Chalker and Owen Brad Spiller.

This study was partly funded by the Microbiology Society International Development Fund Grant (GA002502). The funding body had no role in the design of the study, collection of data, analysis, interpretation of data, and writing the manuscript.

Open Access: This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this
licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http:// creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

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

Citation: Acolatse, J.E.E., Portal, E.A.R., Boostrom, I. et al. Environmental surveillance of ESBL and carbapenemase-producing gram-negative bacteria in a Ghanaian Tertiary Hospital. Antimicrob Resist Infect Control 11, 49 (2022).

DOI: https://doi.org/10.1186/s13756-022-01090-2

Keywords

AFRICA
AMR
Acinetobacter
CRAB
Carbapenemase
ESBL
Ghana
Hospital environment
Infection prevention and control
NDM

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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Cite this

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title = "Environmental surveillance of ESBL and carbapenemase-producing gram-negative bacteria in a Ghanaian Tertiary Hospital",

abstract = "Background: The burden of antibiotic resistant infection is mainly felt in low-to-middle income countries, where the rate of antimicrobial resistance is largely under-surveyed and under huge pressure from unregulated, disparate and often self-guided access to antimicrobials. Nosocomial infections from hospital environments have been shown to be a particularly prevalent source of multi-drug resistant strains, yet surveillance of hospital environmental contamination is often not investigated. Methods: The study was prospective, observational and cross-sectional, sampling 231 high and low touch surfaces from 15th March to 13th April 2021, from five wards in the Cape Coast Teaching Hospital, Ghana. Microbial growth in the presence of vancomycin and either meropenem or cefotaxime was examined and bacterial species were identified by MALDI-TOF. The presence of common extended-spectrum β-lactamases (ESBL) and carbapenemase antimicrobial resistance genes (ARG) were identified through PCR screening, which were confirmed by phenotypic antimicrobial susceptibility determination. Isolates positive for carbapenem resistance genes were sequenced using a multi-platform approach. Results: We recovered microbial growth from 99% of swabs (n = 229/231) plated on agar in the absence of antimicrobials. Multiple sites were found to be colonised with resistant bacteria throughout the hospital setting. Bacteria with multi-drug resistance and ARG of concern were isolated from high and low touch points with evidence of strain dissemination throughout the environment. A total of 21 differing species of bacteria carrying ARG were isolated. The high prevalence of Acinetobacter baumannii carrying blaNDM-1 observed was further characterised by whole genome sequencing and phylogenetic analysis to determine the relationship between resistant strains found in different wards. Conclusion: Evidence of multiple clonal incursions of MDR bacteria of high sepsis risk were found in two separate wards for a regional hospital in Ghana. The prevalence of multiple blaNDM carrying species in combination with combinations of ESBLs was particularly concerning and unexpected in Africa. We also identify strains carrying tet(X3), blaVIM-5 or blaDIM-1 showing a high diversity of carbapenamases present as a reservoir in a hospital setting. Findings of multi-drug resistant bacteria from multiple environmental sites throughout the hospital will inform future IPC practices and aid research prioritisation for AMR in Ghana.",

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author = "Acolatse, {Joseph Elikem Efui} and Portal, {Edward A.R.} and Ian Boostrom and George Akafity and Dakroah, {Mavis Puopelle} and Chalker, {Victoria J.} and Kirsty Sands and Spiller, {Owen B.}",

note = "Funding Information: We are grateful to the Chief Executive, the Laboratory manager, and all the nurse-in-charges of the various wards sampled in the Cape Coast Teaching Hospital for their support during this study. We are thankful to Dr Maria Mendes De Carvalho for the development of the CTX-M-15 PCR and to Dr Brekhna Hassan for developing the carbapenemase multiplex PCR (data unpublished). We would like to thank the NHS staff in the Specialist Antimicrobial Chemotherapy Unit (SACU) Public Health Wales for supporting access to the MALDI-TOF MS instrument. Bioinformatics analysis was undertaken using the supercomputing facilities at Cardiff University operated by Advanced Research Computing at Cardiff (ARCCA) on behalf of the Cardiff Supercomputing Facility and the HPC Wales and Supercomputing Wales (SCW) projects. We acknowledge the support of the latter, which is part-funded by the European Regional Development Fund (ERDF) via the Welsh Government. Joseph Elikem Efui Acolatse has received support and guidance for the study/project through ESCMID's mentorship programme by Victoria J. Chalker and Owen Brad Spiller. This study was partly funded by the Microbiology Society International Development Fund Grant (GA002502). The funding body had no role in the design of the study, collection of data, analysis, interpretation of data, and writing the manuscript. Open Access: This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article{\textquoteright}s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article{\textquoteright}s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http:// creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Publisher Copyright: {\textcopyright} 2022, The Author(s). Citation: Acolatse, J.E.E., Portal, E.A.R., Boostrom, I. et al. Environmental surveillance of ESBL and carbapenemase-producing gram-negative bacteria in a Ghanaian Tertiary Hospital. Antimicrob Resist Infect Control 11, 49 (2022). DOI: https://doi.org/10.1186/s13756-022-01090-2",

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T1 - Environmental surveillance of ESBL and carbapenemase-producing gram-negative bacteria in a Ghanaian Tertiary Hospital

AU - Acolatse, Joseph Elikem Efui

AU - Portal, Edward A.R.

AU - Boostrom, Ian

AU - Akafity, George

AU - Dakroah, Mavis Puopelle

AU - Chalker, Victoria J.

AU - Sands, Kirsty

AU - Spiller, Owen B.

N1 - Funding Information: We are grateful to the Chief Executive, the Laboratory manager, and all the nurse-in-charges of the various wards sampled in the Cape Coast Teaching Hospital for their support during this study. We are thankful to Dr Maria Mendes De Carvalho for the development of the CTX-M-15 PCR and to Dr Brekhna Hassan for developing the carbapenemase multiplex PCR (data unpublished). We would like to thank the NHS staff in the Specialist Antimicrobial Chemotherapy Unit (SACU) Public Health Wales for supporting access to the MALDI-TOF MS instrument. Bioinformatics analysis was undertaken using the supercomputing facilities at Cardiff University operated by Advanced Research Computing at Cardiff (ARCCA) on behalf of the Cardiff Supercomputing Facility and the HPC Wales and Supercomputing Wales (SCW) projects. We acknowledge the support of the latter, which is part-funded by the European Regional Development Fund (ERDF) via the Welsh Government. Joseph Elikem Efui Acolatse has received support and guidance for the study/project through ESCMID's mentorship programme by Victoria J. Chalker and Owen Brad Spiller. This study was partly funded by the Microbiology Society International Development Fund Grant (GA002502). The funding body had no role in the design of the study, collection of data, analysis, interpretation of data, and writing the manuscript. Open Access: This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http:// creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Publisher Copyright: © 2022, The Author(s). Citation: Acolatse, J.E.E., Portal, E.A.R., Boostrom, I. et al. Environmental surveillance of ESBL and carbapenemase-producing gram-negative bacteria in a Ghanaian Tertiary Hospital. Antimicrob Resist Infect Control 11, 49 (2022). DOI: https://doi.org/10.1186/s13756-022-01090-2

PY - 2022/3/16

Y1 - 2022/3/16

N2 - Background: The burden of antibiotic resistant infection is mainly felt in low-to-middle income countries, where the rate of antimicrobial resistance is largely under-surveyed and under huge pressure from unregulated, disparate and often self-guided access to antimicrobials. Nosocomial infections from hospital environments have been shown to be a particularly prevalent source of multi-drug resistant strains, yet surveillance of hospital environmental contamination is often not investigated. Methods: The study was prospective, observational and cross-sectional, sampling 231 high and low touch surfaces from 15th March to 13th April 2021, from five wards in the Cape Coast Teaching Hospital, Ghana. Microbial growth in the presence of vancomycin and either meropenem or cefotaxime was examined and bacterial species were identified by MALDI-TOF. The presence of common extended-spectrum β-lactamases (ESBL) and carbapenemase antimicrobial resistance genes (ARG) were identified through PCR screening, which were confirmed by phenotypic antimicrobial susceptibility determination. Isolates positive for carbapenem resistance genes were sequenced using a multi-platform approach. Results: We recovered microbial growth from 99% of swabs (n = 229/231) plated on agar in the absence of antimicrobials. Multiple sites were found to be colonised with resistant bacteria throughout the hospital setting. Bacteria with multi-drug resistance and ARG of concern were isolated from high and low touch points with evidence of strain dissemination throughout the environment. A total of 21 differing species of bacteria carrying ARG were isolated. The high prevalence of Acinetobacter baumannii carrying blaNDM-1 observed was further characterised by whole genome sequencing and phylogenetic analysis to determine the relationship between resistant strains found in different wards. Conclusion: Evidence of multiple clonal incursions of MDR bacteria of high sepsis risk were found in two separate wards for a regional hospital in Ghana. The prevalence of multiple blaNDM carrying species in combination with combinations of ESBLs was particularly concerning and unexpected in Africa. We also identify strains carrying tet(X3), blaVIM-5 or blaDIM-1 showing a high diversity of carbapenamases present as a reservoir in a hospital setting. Findings of multi-drug resistant bacteria from multiple environmental sites throughout the hospital will inform future IPC practices and aid research prioritisation for AMR in Ghana.

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KW - AMR

KW - Acinetobacter

KW - CRAB

KW - Carbapenemase

KW - ESBL

KW - Ghana

KW - Hospital environment

KW - Infection prevention and control

KW - NDM

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U2 - 10.1186/s13756-022-01090-2

DO - 10.1186/s13756-022-01090-2

M3 - Article

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AN - SCOPUS:85126714397

SN - 2047-2994

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JO - Antimicrobial Resistance and Infection Control

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ER -

Environmental surveillance of ESBL and carbapenemase-producing gram-negative bacteria in a Ghanaian Tertiary Hospital

Abstract

Bibliographical note

Keywords

UN SDGs

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