Evidence map›Paper›PMID 31891609›Full record

ArticlePloS one2019

Decreasing prevalence of contamination with extended-spectrum beta-lactamase-producing Enterobacteriaceae (ESBL-E) in retail chicken meat in the Netherlands.

Pepijn Huizinga, Marjolein Kluytmans-van den Bergh, John W Rossen, Ina Willemsen, Carlo Verhulst, Paul H M Savelkoul, Alexander W Friedrich, Silvia García-Cobos, Jan Kluytmans

Abstract read
In one paragraph

Article in PloS one, 2019. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 13 papers.

0numbers the graph read from it
0cells of the map it votes in
13citing papers in PubMed
–field-weighted citation impact
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

13 citing papers in PubMed.

  1. Article
  2. Review
  3. Review
  4. One Health genomic surveillance ofFrontiers in microbiology · 2026
    Article
  5. Article
  6. Isolation of ESBL-ProducingMicroorganisms · 2025
    Article
  7. Review
  8. Review
  9. Article
  10. Raw Meat Contaminated with Cephalosporin-ResistantMolecules (Basel, Switzerland) · 2022
    Article
  11. Article
  12. Prevalence and Characterization of ESBL/AmpC ProducingAntibiotics (Basel, Switzerland) · 2021
    Article
  13. Identification of a Cluster of Extended-spectrum Beta-Lactamase-Producing Klebsiella pneumoniae Sequence Type 101 Isolated From Food and Humans.Clinical infectious diseases : an official publication of the Infectious Diseases Society of America · 2021
    Article
4 · The record

Corrections and comments

PubMed lists nothing against this paper. Absence here is not a guarantee, only a check that was made.

5 · Who and what money

Authors and funding

9 authors.

Pepijn HuizingaDepartment of Infection Control, Amphia Hospital, Breda, the Netherlands.ORCID 0000-0001-8107-8667
Marjolein Kluytmans-van den BerghDepartment of Infection Control, Amphia Hospital, Breda, the Netherlands.
John W RossenUniversity of Groningen, University Medical Center Groningen, Department of Medical Microbiology and Infection Prevention, Groningen, the Netherlands.
Ina WillemsenDepartment of Infection Control, Amphia Hospital, Breda, the Netherlands.
Carlo VerhulstDepartment of Infection Control, Amphia Hospital, Breda, the Netherlands.
Paul H M SavelkoulMaastricht University Medical Center, Caphri School for Public Health and Primary Care, Department of Medical Microbiology, Maastricht, the Netherlands.
Alexander W FriedrichUniversity of Groningen, University Medical Center Groningen, Department of Medical Microbiology and Infection Prevention, Groningen, the Netherlands.
Silvia García-CobosUniversity of Groningen, University Medical Center Groningen, Department of Medical Microbiology and Infection Prevention, Groningen, the Netherlands.
Jan KluytmansDepartment of Infection Control, Amphia Hospital, Breda, the Netherlands.

Funding

Wellcome Trust
6 · The paper itself

Abstract

Retail chicken meat is a potential source of extended-spectrum beta-lactamase-producing Enterobacteriaceae (ESBL-E). In the past decade, vast national efforts were undertaken to decrease the antibiotic use in the veterinary sector, resulting in a 58% decrease in antibiotic sales in the sector between 2009 and 2014. This decrease in antibiotic use was followed by a decrease in ESBL-E prevalence in broilers. The current study investigates the prevalence of contamination with ESBL-E in retail chicken meat purchased in the Netherlands between December 2013 and August 2015. It looks at associations between the prevalence of contamination with ESBL-E and sample characteristics such as method of farming (free-range or conventional), supermarket chain of purchase and year of purchase. In the current study, 352 chicken meat samples were investigated for the presence of ESBL-E using selective culture methods. Six samples were excluded due to missing isolates or problems obtaining a good quality sequence leaving 346 samples for further analyses. Of these 346 samples, 188 (54.3%) were positive for ESBL-E, yielding 216 ESBL-E isolates (Escherichia coli (n = 204), Klebsiella pneumoniae (n = 11) and Escherichia fergusonii (n = 1)). All ESBL-E isolates were analysed using whole-genome sequencing. The prevalence of contamination with ESBL-E in retail chicken meat decreased from 68.3% in 2014 to 44.6% in 2015, absolute risk difference 23.7% (95% confidence interval (CI): 12.6% - 34.1%). The ESBL-E prevalence was lower in free-range chicken meat (36.4%) compared with conventional chicken meat (61.5%), absolute risk difference 25.2% (95% CI: 12.9% - 36.5%). The prevalence of contamination with ESBL-E varied between supermarket chains, the highest prevalence of contamination was found in supermarket chain 4 (76.5%) and the lowest in supermarket chain 1 (37.8%). Pairwise isolate comparisons using whole-genome multilocus sequence typing (wgMLST) showed that clustering of isolates occurs more frequently within supermarket chains than between supermarket chains. In conclusion, the prevalence of contamination with ESBL-E in retail chicken in the Netherlands decreased over time; nevertheless, it remains substantial and as such a potential source for ESBL-E in humans.

Indexed as

AnimalsBacterial Typing Techniquesbeta-LactamasesChickensEscherichia coliFood MicrobiologyKlebsiella pneumoniaeNetherlandsPoultry Productsbeta-Lactamases

Identifiers

PMID31891609
PMCPMC6938319

What OpenQuestion holds

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Registered trials

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Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.