Antimicrobial resistance genes aph(3')-III, erm(B), sul2 and tet(W) abundance in animal faeces, meat, production environments and human faeces in Europe - PubMed (original) (raw)

. 2022 Jun 29;77(7):1883-1893.

doi: 10.1093/jac/dkac133.

Dick J J Heederik 1, Peter Scherpenisse 1, Liese Van Gompel 1, Roosmarijn E C Luiken 1, Katharina Wadepohl 2, Magdalena Skarżyńska 3, Eri Van Heijnsbergen 1, Inge M Wouters 1, Gerdit D Greve 1, Betty G M Jongerius-Gortemaker 1, Monique Tersteeg-Zijderveld 1, Lützen Portengen 1, Katharina Juraschek 4, Jennie Fischer 4, Magdalena Zając 3, Dariusz Wasyl 3, Jaap A Wagenaar 5, Dik J Mevius 5 6, Lidwien A M Smit 1, Heike Schmitt 1 7

Affiliations

Antimicrobial resistance genes aph(3')-III, erm(B), sul2 and tet(W) abundance in animal faeces, meat, production environments and human faeces in Europe

Dongsheng Yang et al. J Antimicrob Chemother. 2022.

Abstract

Background: Real-time quantitative PCR (qPCR) is an affordable method to quantify antimicrobial resistance gene (ARG) targets, allowing comparisons of ARG abundance along animal production chains.

Objectives: We present a comparison of ARG abundance across various animal species, production environments and humans in Europe. AMR variation sources were quantified. The correlation of ARG abundance between qPCR data and previously published metagenomic data was assessed.

Methods: A cross-sectional study was conducted in nine European countries, comprising 9572 samples. qPCR was used to quantify abundance of ARGs [aph(3')-III, erm(B), sul2, tet(W)] and 16S rRNA. Variance component analysis was conducted to explore AMR variation sources. Spearman's rank correlation of ARG abundance values was evaluated between pooled qPCR data and earlier published pooled metagenomic data.

Results: ARG abundance varied strongly among animal species, environments and humans. This variation was dominated by between-farm variation (pigs) or within-farm variation (broilers, veal calves and turkeys). A decrease in ARG abundance along pig and broiler production chains ('farm to fork') was observed. ARG abundance was higher in farmers than in slaughterhouse workers, and lowest in control subjects. ARG abundance showed a high correlation (Spearman's ρ > 0.7) between qPCR data and metagenomic data of pooled samples.

Conclusions: qPCR analysis is a valuable tool to assess ARG abundance in a large collection of livestock-associated samples. The between-country and between-farm variation of ARG abundance could partially be explained by antimicrobial use and farm biosecurity levels. ARG abundance in human faeces was related to livestock antimicrobial resistance exposure.

© The Author(s) 2022. Published by Oxford University Press on behalf of British Society for Antimicrobial Chemotherapy.

PubMed Disclaimer

Figures

Figure 1.

Figure 1.

Relative abundance of four targets [aph(3′)-III, erm(B), sul2, tet(W)] in all samples. Relative abundance of gene target was calculated by log10 (gene copies/16S copies). Asterisk shows the mean by sample type. Pooled faeces, slaughterhouse pig and broiler faeces, and slaughterhouse carcass samples were not included in this figure.

Figure 2.

Figure 2.

Relative abundance of four targets [aph(3′)-III, erm(B), sul2, tet(W)] in samples related to pig production in the Netherlands. Relative abundance of gene target was calculated by log10 (gene copies/16S copies). Only pig farms and slaughterhouses in the Netherlands were involved. Human faeces of control subjects were collected from the ‘Lifelines’ cohort in the Netherlands. Asterisk shows the mean by sample type in the Netherlands.

Figure 3.

Figure 3.

Relative abundance of four targets [aph(3′)-III, erm(B), sul2, tet(W)] in samples related to broiler production in Germany. Relative abundance of gene target was calculated by log10 (gene copies/16S copies). Only broiler farms and slaughterhouses in Germany were involved. Asterisk shows the mean by sample type in Germany.

Figure 4.

Figure 4.

PCA biplot of relative ARG abundance in animal faecal samples. ARG targets: aph(3′)-III, erm(B), sul2, tet(W). Relative abundance of gene target was calculated by log10 (gene copies/16S copies). Symmetric scaling was used. Circles indicate 95% confidence ellipses that were computed with the assumption of multivariate normal distribution of the data.

Figure 5.

Figure 5.

Variance component percentages of relative ARG abundance in faecal samples from pigs and broilers. Relative abundance of gene target was calculated by log10 (gene copies/16S copies). Variance percentages of three components (between-country variance, between-farm variance and within-farm variance) were calculated using VCA.

Figure 6.

Figure 6.

Spearman’s rank correlation of relative ARG abundance and ARG FPKM abundance in pooled faecal samples from pig and broiler farms. ARG targets: aph(3′)-III, erm(B), sul2, tet(W). Relative abundance of gene target was calculated by log10 (gene copies/16S copies). FPKM was log10 transformed after adding a pseudocount of 1. BE, Belgium; BG, Bulgaria; DE, Germany; DK, Denmark; ES, Spain; FR, France; IT, Italy; NL, the Netherlands; PL, Poland.

Similar articles

Cited by

References

    1. WHO . Antimicrobial resistance: global report on surveillance. 2014. https://apps.who.int/iris/handle/10665/112642.
    1. CLSI . Performance Standards for Antimicrobial Susceptibility Testing—Twentieth Edition: M100. 2011.
    1. CLSI . Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals—Fourth Edition: VET01. 2013.
    1. Munk P, Knudsen BE, Lukjancenko Oet al. . Abundance and diversity of the faecal resistome in slaughter pigs and broilers in nine European countries. Nat Microbiol 2018; 3: 898–908. - PubMed
    1. Van Gompel L, Luiken RE, Sarrazin Set al. . The antimicrobial resistome in relation to antimicrobial use and biosecurity in pig farming, a metagenome-wide association study in nine European countries. J Antimicrob Chemother 2019; 74: 865–76. - PubMed

Publication types

MeSH terms

Substances

LinkOut - more resources