Performance of CHROMagar ESBL media for the surveillance of extended-spectrum cephalosporin-resistant Enterobacterales (ESCrE) from rectal swabs in Botswana

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Abstract

Introduction. Lack of laboratory capacity hampers consistent national antimicrobial resistance (AMR) surveillance. Chromogenic media may provide a practical screening tool for detection of individuals colonized by extended-spectrum beta-lactamase (ESBL)-producing organisms.

Hypothesis. CHROMagar ESBL media represent an adequate screening method for the detection of extended-spectrum cephalosporin-resistant Enterobacterales (ESCrE), isolated from rectal swabs.

Aim. To evaluate the performance of CHROMagar ESBL media to accurately identify ESCrE isolates from rectal swab samples attained from hospitalized and community participants.

Methodology. All participants provided informed consent prior to enrolment. Rectal swabs from 2469 hospital and community participants were inoculated onto CHROMagar ESBL. The performance of CHROMagar ESBL to differentiate Escherichia coli and Klebsiella spp., Enterobacter spp. and Citrobacter spp. (KEC spp.) as well as select for extended-spectrum cephalosporin resistance were compared to matrix-assisted laser desorption/ionization-time-of-flight MS (MALDI-TOF-MS) and VITEK-2 automated susceptibility testing.

Results. CHROMagar ESBL had a positive and negative agreement of 91.2 % (95 % CI, 88.4–93.3) and 86.8 % (95 % CI, 82.0–90.7) for E. coli and 88.1 % (95 % CI 83.2–92.1) and 87.6 % (95 % CI 84.7–90.2) for KEC spp. differentiation, respectively, when compared to species ID by MALDI-TOF-MS. When evaluated for phenotypic susceptibilities (VITEK-2), 88.1 % (714/810) of the isolates recovered on the selective agar exhibited resistance to third-generation cephalosporins.

Conclusion. The performance characteristics of CHROMagar ESBL media suggest that they may be a viable screening tool for the identification of ESCrE from hospitalized and community participants and could be used to inform infection prevention and control practices in Botswana and potentially other low-and middle-income countries (LMICs). Further studies are required to analyse the costs and the impact on time-to-result of the media in comparison with available laboratory methods for ESCrE surveillance in the country.

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Most cited references 21

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Burden of endemic health-care-associated infection in developing countries: systematic review and meta-analysis.

Benedetta Allegranzi, Sepideh Bagheri Nejad, Christophe Combescure … (2011)

Health-care-associated infection is the most frequent result of unsafe patient care worldwide, but few data are available from the developing world. We aimed to assess the epidemiology of endemic health-care-associated infection in developing countries. We searched electronic databases and reference lists of relevant papers for articles published 1995-2008. Studies containing full or partial data from developing countries related to infection prevalence or incidence-including overall health-care-associated infection and major infection sites, and their microbiological cause-were selected. We classified studies as low-quality or high-quality according to predefined criteria. Data were pooled for analysis. Of 271 selected articles, 220 were included in the final analysis. Limited data were retrieved from some regions and many countries were not represented. 118 (54%) studies were low quality. In general, infection frequencies reported in high-quality studies were greater than those from low-quality studies. Prevalence of health-care-associated infection (pooled prevalence in high-quality studies, 15·5 per 100 patients [95% CI 12·6-18·9]) was much higher than proportions reported from Europe and the USA. Pooled overall health-care-associated infection density in adult intensive-care units was 47·9 per 1000 patient-days (95% CI 36·7-59·1), at least three times as high as densities reported from the USA. Surgical-site infection was the leading infection in hospitals (pooled cumulative incidence 5·6 per 100 surgical procedures), strikingly higher than proportions recorded in developed countries. Gram-negative bacilli represented the most common nosocomial isolates. Apart from meticillin resistance, noted in 158 of 290 (54%) Staphylococcus aureus isolates (in eight studies), very few articles reported antimicrobial resistance. The burden of health-care-associated infection in developing countries is high. Our findings indicate a need to improve surveillance and infection-control practices. World Health Organization. Copyright Â© 2011 Elsevier Ltd. All rights reserved.

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Trends in human fecal carriage of extended-spectrum β-lactamases in the community: toward the globalization of CTX-M.

P-L Woerther, C Burdet, E Chachaty … (2013)

In the last 10 years, extended-spectrum β-lactamase-producing enterobacteria (ESBL-E) have become one of the main challenges for antibiotic treatment of enterobacterial infections, largely because of the current CTX-M enzyme pandemic. However, most studies have focused on hospitalized patients, though today it appears that the community is strongly affected as well. We therefore decided to devote our investigation to trends in ESBL-E fecal carriage rates and comprehensively reviewed data from studies conducted on healthy populations in various parts of the world. We show that (i) community ESBL-E fecal carriage, which was unknown before the turn of the millennium, has since increased significantly everywhere, with developing countries being the most affected; (ii) intercontinental travel may have emphasized and globalized the issue; and (iii) CTX-M enzymes, especially CTX-M-15, are the dominant type of ESBL. Altogether, these results suggest that CTX-M carriage is evolving toward a global pandemic but is still insufficiently described. Only a better knowledge of its dynamics and biology will lead to further development of appropriate control measures.

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Extended-spectrum-β-lactamase- and AmpC-β-lactamase-producing Escherichia coli in Dutch broilers and broiler farmers.

Dik Mevius, Alieda van Essen-Zandbergen, Rene van der Heijden … (2012)

The aim of this study was to establish the prevalence of extended-spectrum β-lactamase (ESBL)- and AmpC β-lactamase-producing Escherichia coli at Dutch broiler farms and in farmers and to compare ESBL/AmpC-producing isolates from farmers and their animals. Twenty-five to 41 cloacal swabs collected from broilers at each of 26 farms and 18 faecal samples from 18 broiler farmers were analysed for determination of the presence of ESBL/AmpC-producing E. coli. ESBL/AmpC genes were characterized by microarray, PCR and sequencing. Plasmids were characterized by transformation and PCR-based replicon typing. Subtyping of plasmids was done by plasmid multilocus sequence typing or restriction fragment length polymorphism. E. coli genotypes were determined by multilocus sequence typing. Birds from all farms were positive for ESBL/AmpC-producing E. coli, and on 22/26 farms the within-farm prevalence was ≥ 80%. Six of 18 farmers carried isolates containing ESBL/AmpC genes bla(CTX-M-1), bla(CMY-2) and/or bla(SHV-12), which were also present in the samples from their animals. In five of these isolates, the genes were located on identical plasmid families [IncI1 (n = 3), IncK (n = 1) or IncN (n = 1)], and in isolates from two farmers the genes were carried on identical plasmid subtypes (IncI1 ST12 and IncN ST1, where ST stands for sequence type) as in the isolates from their animals. This study shows a high prevalence of birds carrying ESBL/AmpC-producing E. coli at Dutch broiler farms and a high prevalence of ESBL/AmpC-producing E. coli in farmers. This is undesirable due to the risk this poses to human health. Future research should focus on identification of the source of these isolates in the broiler production chain to make interventions resulting in reduction of these isolates possible.

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Author and article information

Contributors

Naledi Mannathoko:

ORCID: http://orcid.org/0000-0002-9429-2838

Ebbing Lautenbach

Mosepele Mosepele

Dimpho Otukile

Kgotlaetsile Sewawa

Laurel Glaser

Leigh Cressman

Laura Cowden

Kevin Alby

Anne Jaskowiak-Barr

Robert Gross

Margaret Mokomane

Giacomo M. Paganotti

Ashley Styczynski

Rachel M. Smith

Evan Snitkin

Tiffany Wan

Warren B. Bilker

Melissa Richard-Greenblatt

Journal

Journal ID (nlm-ta): J Med Microbiol

Journal ID (iso-abbrev): J Med Microbiol

Journal ID (hwp): jmm

Journal ID (publisher-id): jmm

Title: Journal of Medical Microbiology

Publisher: Microbiology Society

ISSN (Print): 0022-2615

ISSN (Electronic): 1473-5644

Publication date Collection: 2023

Publication date (Electronic): 22 November 2023

Publication date PMC-release: 22 November 2023

Volume: 72

Issue: 11

Electronic Location Identifier: 001770

Affiliations

[1 ]departmentDepartment of Biomedical Sciences , University of Botswana , Gaborone, Botswana

[2 ]Center for Clinical Epidemiology and Biostatistics, Perelman School of Medicine, University of Pennsylvania , Philadelphia, PA, USA

[3 ]departmentDivision of Infectious Diseases, Department of Medicine , Perelman School of Medicine, University of Pennsylvania , Philadelphia, PA, USA

[4 ]departmentDepartment of Biostatistics, Epidemiology, and Informatics , Perelman School of Medicine, University of Pennsylvania , Philadelphia, PA, USA

[5 ]departmentDepartment of Internal Medicine , University of Botswana , Gaborone, Botswana

[6 ]Botswana-University of Pennsylvania Partnership (BUP) , Gaborone, Botswana

[7 ]departmentDepartment of Pathology and Laboratory Medicine , University Pennsylvania , Philadelphia, PA, USA

[8 ]departmentDepartment of Pathology and Laboratory Medicine , University of North Carolina , Chapel Hill, NC, USA

[9 ]departmentDepartment of Biomedical Sciences , University of Botswana , Gaborone, Botswana

[10 ]Centers for Disease Control and Prevention (CDC) , Atlanta, GA, USA

[11 ]departmentDepartment of Microbiology and Immunology , University of Michigan , Ann Arbor, Michigan, USA

[12 ]departmentDepartment of Laboratory Medicine and Pathobiology , University of Toronto , ON, Canada

[13 ]Hospital for Sick Children , Toronto, Ontario, Canada

Author notes

MelissaRichard-Greenblatt, melissa.greenblatt@ 123456sickkids.ca

The authors report no conflicts of interest.

Supplement: Three supplementary tables are available with the online version of this article.

Author information

Naledi Mannathoko http://orcid.org/0000-0002-9429-2838

Article

Publisher ID: 001770

DOI: 10.1099/jmm.0.001770

PMC ID: 11145880

PubMed ID: 37991431

SO-VID: 227ea845-a983-419d-b468-d75aef15843c

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution License.

History

Date received : 05 September 2023

Date accepted : 13 October 2023

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Performance of CHROMagar ESBL media for the surveillance of extended-spectrum cephalosporin-resistant Enterobacterales (ESCrE) from rectal swabs in Botswana

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Most cited references 21

Burden of endemic health-care-associated infection in developing countries: systematic review and meta-analysis.

Trends in human fecal carriage of extended-spectrum β-lactamases in the community: toward the globalization of CTX-M.

Extended-spectrum-β-lactamase- and AmpC-β-lactamase-producing Escherichia coli in Dutch broilers and broiler farmers.

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