Evaluation of screening algorithms to detect rectal colonization with carbapenemase-producing Enterobacterales in a resource-limited setting

Thi Anh Mai Pham; Tung Xuan Nguyen; Troung Nhat My; Lan Thi Le; Huyen Thi Vu; Ngoc Thi Bich Hoang; Dien M. Tran; Linh Viet Nguyen; Phuc D. Pham; Dennis Nurjadi; Flavie Goutard; Thirumalaisamy P. Velavan; Van Anh Thi Dinh; Y. M.Gildas Hounmanou; Bent Jörgensen; Le Huu Song; Nhung T.T. Nguyen; Etienne Loire; Åse Östholm; Lennart E. Nilsson; Tuyet Hanh T. Tran; Phuc H. Phan; Anders Dalsgaard; Mattias Larsson; Linus Olson; Håkan Hanberger

doi:10.1093/jacamr/dlae089

Evaluation of screening algorithms to detect rectal colonization with carbapenemase-producing Enterobacterales in a resource-limited setting

Thi Anh Mai Pham, Tung Xuan Nguyen, Troung Nhat My, Lan Thi Le, Huyen Thi Vu, Ngoc Thi Bich Hoang, Dien M. Tran, Linh Viet Nguyen, Phuc D. Pham, Dennis Nurjadi, Flavie Goutard, Thirumalaisamy P. Velavan, Van Anh Thi Dinh, Y. M.Gildas Hounmanou, Bent Jörgensen, Le Huu Song, Nhung T.T. Nguyen, Etienne Loire, Åse Östholm, Lennart E. NilssonTuyet Hanh T. Tran, Phuc H. Phan, Anders Dalsgaard, Mattias Larsson, Linus Olson^*, Håkan Hanberger

^*Corresponding author af dette arbejde

Sektion, Food Safety and Zoonoses

Publikation: Bidrag til tidsskrift › Tidsskriftartikel › Forskning › peer review

1 Citationer (Scopus)

15 Downloads (Pure)

Abstract

Objectives: To improve and rationalize the detection of carbapenemase-producing Enterobacterales (CPE) in rectal swabs in a high-prevalence and resource-constrained setting, addressing surveillance challenges typically encountered in laboratories with limited resources. Methods: A point prevalence survey (PPS) was conducted on 15 August 2022, in a provincial children's hospital in northern Vietnam. Rectal swab samples of all admitted children were collected and plated on a selective medium for carbapenem-resistant Enterobacterales (CRE). Species identification and antimicrobial susceptibility testing (AST) were performed by MALDI-TOF, and VITEK2 XL and interpreted according to CLSI breakpoints (2022). Carbapenemases were detected by the carbapenem inactivation method (CIM) and quantitative real-time PCR (qRT-PCR). Results: Rectal swab samples were obtained from 376 patients. Of 178 isolates growing on the CRE screening agar, 140 isolates were confirmed as Enterobacterales of which 118 (84.3%) isolates were resistant to meropenem and/or ertapenem. CIM and PCR showed that 90/118 (76.3%) were carbapenemase producers. Overall, 83/367 (22.6%) were colonized by CPE. Klebsiella pneumoniae, Escherichia coli and Enterobacter cloacae complex were the most common CPE detected, with NDM as the predominant carbapenemase (78/90; 86.7%). Phenotypic resistance to meropenem was the best predictor of CPE production (sensitivity 85.6%, specificity 100%) compared with ertapenem resistance (95.6% sensitivity, 36% specificity). CIM was 100% concordant with PCR in detecting carbapenemases. Conclusions: These findings underscore the effectiveness of meropenem resistance as a robust indicator of the production of carbapenemases and the reliability of the CIM method to detect such carbapenemases in resource-limited settings where the performance of molecular methods is not possible.

Originalsprog	Engelsk
Artikelnummer	dlae089
Tidsskrift	JAC-Antimicrobial Resistance
Vol/bind	6
Udgave nummer	3
Antal sider	6
ISSN	2632-1823
DOI	https://doi.org/10.1093/jacamr/dlae089
Status	Udgivet - 2024

Bibliografisk note

Funding Information:
This project received funding from the Swedish Research Council (VR), Federal Ministry of Education and Research, Germany (BMBF), the French National Research Agency (ANR), Innovation Fund Denmark (IFD), and the International Centre for Antimicrobial Resistance Solutions (ICARS) under the umbrella of the JPIAMR (Joint Programming Initiative on Antimicrobial Resistance).

Funding Information:
The I-CRECT (Intervention to decrease CRE Colonization and Transmission between hospitals, households, communities and domesticated animals) group would like to thank the Joint Programming Initiative on Antimicrobial Resistance (JPIAMR). The I-CRECT team consists of the members/partners below. The project acknowledges and is thankful for the funding, mentioned in the Funding section, that has made the project possible. We thank all participants, households, hospitals and local authorities for their collaboration. Especial thanks go to the Thai Binh Pediatric Hospital and their staff that helped during the PPS. We also acknowledge and thank the staff at the Vietnamese-German Center for Medical Research and the research group of Dennis Nurjadi who supported with external validation of the initial findings

Publisher Copyright:
© 2024 The Author(s). Published by Oxford University Press on behalf of British Society for Antimicrobial Chemotherapy.

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10.1093/jacamr/dlae089Licens: CC BY-NC

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Citationsformater

Pham, T. A. M., Nguyen, T. X., My, T. N., Le, L. T., Vu, H. T., Hoang, N. T. B., Tran, D. M., Nguyen, L. V., Pham, P. D., Nurjadi, D., Goutard, F., Velavan, T. P., Dinh, V. A. T., Hounmanou, Y. M. G., Jörgensen, B., Song, L. H., Nguyen, N. T. T., Loire, E., Östholm, Å., ... Hanberger, H. (2024). Evaluation of screening algorithms to detect rectal colonization with carbapenemase-producing Enterobacterales in a resource-limited setting. JAC-Antimicrobial Resistance, 6(3), Artikel dlae089. https://doi.org/10.1093/jacamr/dlae089

Pham, TAM, Nguyen, TX, My, TN, Le, LT, Vu, HT, Hoang, NTB, Tran, DM, Nguyen, LV, Pham, PD, Nurjadi, D, Goutard, F, Velavan, TP, Dinh, VAT, Hounmanou, YMG, Jörgensen, B, Song, LH, Nguyen, NTT, Loire, E, Östholm, Å, Nilsson, LE, Tran, THT, Phan, PH, Dalsgaard, A, Larsson, M, Olson, L & Hanberger, H 2024, 'Evaluation of screening algorithms to detect rectal colonization with carbapenemase-producing Enterobacterales in a resource-limited setting', JAC-Antimicrobial Resistance, bind 6, nr. 3, dlae089. https://doi.org/10.1093/jacamr/dlae089

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title = "Evaluation of screening algorithms to detect rectal colonization with carbapenemase-producing Enterobacterales in a resource-limited setting",

abstract = "Objectives: To improve and rationalize the detection of carbapenemase-producing Enterobacterales (CPE) in rectal swabs in a high-prevalence and resource-constrained setting, addressing surveillance challenges typically encountered in laboratories with limited resources. Methods: A point prevalence survey (PPS) was conducted on 15 August 2022, in a provincial children's hospital in northern Vietnam. Rectal swab samples of all admitted children were collected and plated on a selective medium for carbapenem-resistant Enterobacterales (CRE). Species identification and antimicrobial susceptibility testing (AST) were performed by MALDI-TOF, and VITEK2 XL and interpreted according to CLSI breakpoints (2022). Carbapenemases were detected by the carbapenem inactivation method (CIM) and quantitative real-time PCR (qRT-PCR). Results: Rectal swab samples were obtained from 376 patients. Of 178 isolates growing on the CRE screening agar, 140 isolates were confirmed as Enterobacterales of which 118 (84.3%) isolates were resistant to meropenem and/or ertapenem. CIM and PCR showed that 90/118 (76.3%) were carbapenemase producers. Overall, 83/367 (22.6%) were colonized by CPE. Klebsiella pneumoniae, Escherichia coli and Enterobacter cloacae complex were the most common CPE detected, with NDM as the predominant carbapenemase (78/90; 86.7%). Phenotypic resistance to meropenem was the best predictor of CPE production (sensitivity 85.6%, specificity 100%) compared with ertapenem resistance (95.6% sensitivity, 36% specificity). CIM was 100% concordant with PCR in detecting carbapenemases. Conclusions: These findings underscore the effectiveness of meropenem resistance as a robust indicator of the production of carbapenemases and the reliability of the CIM method to detect such carbapenemases in resource-limited settings where the performance of molecular methods is not possible. ",

author = "Pham, {Thi Anh Mai} and Nguyen, {Tung Xuan} and My, {Troung Nhat} and Le, {Lan Thi} and Vu, {Huyen Thi} and Hoang, {Ngoc Thi Bich} and Tran, {Dien M.} and Nguyen, {Linh Viet} and Pham, {Phuc D.} and Dennis Nurjadi and Flavie Goutard and Velavan, {Thirumalaisamy P.} and Dinh, {Van Anh Thi} and Hounmanou, {Y. M.Gildas} and Bent J{\"o}rgensen and Song, {Le Huu} and Nguyen, {Nhung T.T.} and Etienne Loire and {\AA}se {\"O}stholm and Nilsson, {Lennart E.} and Tran, {Tuyet Hanh T.} and Phan, {Phuc H.} and Anders Dalsgaard and Mattias Larsson and Linus Olson and H{\aa}kan Hanberger",

note = "Publisher Copyright: {\textcopyright} 2024 The Author(s). Published by Oxford University Press on behalf of British Society for Antimicrobial Chemotherapy.",

year = "2024",

doi = "10.1093/jacamr/dlae089",

language = "English",

volume = "6",

journal = "JAC-Antimicrobial Resistance",

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TY - JOUR

T1 - Evaluation of screening algorithms to detect rectal colonization with carbapenemase-producing Enterobacterales in a resource-limited setting

AU - Pham, Thi Anh Mai

AU - Nguyen, Tung Xuan

AU - My, Troung Nhat

AU - Le, Lan Thi

AU - Vu, Huyen Thi

AU - Hoang, Ngoc Thi Bich

AU - Tran, Dien M.

AU - Nguyen, Linh Viet

AU - Pham, Phuc D.

AU - Nurjadi, Dennis

AU - Goutard, Flavie

AU - Velavan, Thirumalaisamy P.

AU - Dinh, Van Anh Thi

AU - Hounmanou, Y. M.Gildas

AU - Jörgensen, Bent

AU - Song, Le Huu

AU - Nguyen, Nhung T.T.

AU - Loire, Etienne

AU - Östholm, Åse

AU - Nilsson, Lennart E.

AU - Tran, Tuyet Hanh T.

AU - Phan, Phuc H.

AU - Dalsgaard, Anders

AU - Larsson, Mattias

AU - Olson, Linus

AU - Hanberger, Håkan

PY - 2024

Y1 - 2024

N2 - Objectives: To improve and rationalize the detection of carbapenemase-producing Enterobacterales (CPE) in rectal swabs in a high-prevalence and resource-constrained setting, addressing surveillance challenges typically encountered in laboratories with limited resources. Methods: A point prevalence survey (PPS) was conducted on 15 August 2022, in a provincial children's hospital in northern Vietnam. Rectal swab samples of all admitted children were collected and plated on a selective medium for carbapenem-resistant Enterobacterales (CRE). Species identification and antimicrobial susceptibility testing (AST) were performed by MALDI-TOF, and VITEK2 XL and interpreted according to CLSI breakpoints (2022). Carbapenemases were detected by the carbapenem inactivation method (CIM) and quantitative real-time PCR (qRT-PCR). Results: Rectal swab samples were obtained from 376 patients. Of 178 isolates growing on the CRE screening agar, 140 isolates were confirmed as Enterobacterales of which 118 (84.3%) isolates were resistant to meropenem and/or ertapenem. CIM and PCR showed that 90/118 (76.3%) were carbapenemase producers. Overall, 83/367 (22.6%) were colonized by CPE. Klebsiella pneumoniae, Escherichia coli and Enterobacter cloacae complex were the most common CPE detected, with NDM as the predominant carbapenemase (78/90; 86.7%). Phenotypic resistance to meropenem was the best predictor of CPE production (sensitivity 85.6%, specificity 100%) compared with ertapenem resistance (95.6% sensitivity, 36% specificity). CIM was 100% concordant with PCR in detecting carbapenemases. Conclusions: These findings underscore the effectiveness of meropenem resistance as a robust indicator of the production of carbapenemases and the reliability of the CIM method to detect such carbapenemases in resource-limited settings where the performance of molecular methods is not possible.

AB - Objectives: To improve and rationalize the detection of carbapenemase-producing Enterobacterales (CPE) in rectal swabs in a high-prevalence and resource-constrained setting, addressing surveillance challenges typically encountered in laboratories with limited resources. Methods: A point prevalence survey (PPS) was conducted on 15 August 2022, in a provincial children's hospital in northern Vietnam. Rectal swab samples of all admitted children were collected and plated on a selective medium for carbapenem-resistant Enterobacterales (CRE). Species identification and antimicrobial susceptibility testing (AST) were performed by MALDI-TOF, and VITEK2 XL and interpreted according to CLSI breakpoints (2022). Carbapenemases were detected by the carbapenem inactivation method (CIM) and quantitative real-time PCR (qRT-PCR). Results: Rectal swab samples were obtained from 376 patients. Of 178 isolates growing on the CRE screening agar, 140 isolates were confirmed as Enterobacterales of which 118 (84.3%) isolates were resistant to meropenem and/or ertapenem. CIM and PCR showed that 90/118 (76.3%) were carbapenemase producers. Overall, 83/367 (22.6%) were colonized by CPE. Klebsiella pneumoniae, Escherichia coli and Enterobacter cloacae complex were the most common CPE detected, with NDM as the predominant carbapenemase (78/90; 86.7%). Phenotypic resistance to meropenem was the best predictor of CPE production (sensitivity 85.6%, specificity 100%) compared with ertapenem resistance (95.6% sensitivity, 36% specificity). CIM was 100% concordant with PCR in detecting carbapenemases. Conclusions: These findings underscore the effectiveness of meropenem resistance as a robust indicator of the production of carbapenemases and the reliability of the CIM method to detect such carbapenemases in resource-limited settings where the performance of molecular methods is not possible.

U2 - 10.1093/jacamr/dlae089

DO - 10.1093/jacamr/dlae089

M3 - Journal article

C2 - 38863560

AN - SCOPUS:85196111734

SN - 2632-1823

VL - 6

JO - JAC-Antimicrobial Resistance

JF - JAC-Antimicrobial Resistance

IS - 3

M1 - dlae089

ER -