Azithromycin resistance in Escherichia coli and Salmonella from food-producing animals and meat in Europe

Mirena Ivanova; Armen Ovsepian; Pimlapas Leekitcharoenphon; Anne Mette Seyfarth; Hanne Mordhorst; Saria Otani; Sandra Koeberl-Jelovcan; Mihail Milanov; Gordan Kompes; Maria Liapi; Tomáš Černý; Camilla Thougaard Vester; Agnès Perrin-Guyomard; Jens A Hammerl; Mirjam Grobbel; Eleni Valkanou; Szilárd Jánosi; Rosemarie Slowey; Patricia Alba; Virginia Carfora; Jelena Avsejenko; Asta Pereckiene; Dominique Claude; Renato Zerafa; Kees T Veldman; Cécile Boland; Cristina Garcia-Graells; Pierre Wattiau; Patrick Butaye; Magdalena Zając; Ana Amaro; Lurdes Clemente; Angela M Vaduva; Luminita-Maria Romascu; Nicoleta-Manuela Milita; Andrea Mojžišová; Irena Zdovc; Maria Jesús Zamora Escribano; Cristina De Frutos Escobar; Gudrun Overesch; Christopher Teale; Guy H Loneragan; Beatriz Guerra; Pierre Alexandre Beloeil; Amanda M V Brown; Rene S Hendriksen; Valeria Bortolaia; Jette Sejer Kjeldgaard

doi:10.1093/jac/dkae161

Azithromycin resistance in Escherichia coli and Salmonella from food-producing animals and meat in Europe

Mirena Ivanova, Armen Ovsepian, Pimlapas Leekitcharoenphon, Anne Mette Seyfarth, Hanne Mordhorst, Saria Otani, Sandra Koeberl-Jelovcan, Mihail Milanov, Gordan Kompes, Maria Liapi, Tomáš Černý, Camilla Thougaard Vester, Agnès Perrin-Guyomard, Jens A Hammerl, Mirjam Grobbel, Eleni Valkanou, Szilárd Jánosi, Rosemarie Slowey, Patricia Alba, Virginia CarforaJelena Avsejenko, Asta Pereckiene, Dominique Claude, Renato Zerafa, Kees T Veldman, Cécile Boland, Cristina Garcia-Graells, Pierre Wattiau, Patrick Butaye, Magdalena Zając, Ana Amaro, Lurdes Clemente, Angela M Vaduva, Luminita-Maria Romascu, Nicoleta-Manuela Milita, Andrea Mojžišová, Irena Zdovc, Maria Jesús Zamora Escribano, Cristina De Frutos Escobar, Gudrun Overesch, Christopher Teale, Guy H Loneragan, Beatriz Guerra, Pierre Alexandre Beloeil, Amanda M V Brown, Rene S Hendriksen, Valeria Bortolaia, Jette Sejer Kjeldgaard^*

^*Corresponding author for this work

Research output: Contribution to journal › Journal article › Research › peer-review

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Abstract

Objectives

To characterize the genetic basis of azithromycin resistance in Escherichia coli and Salmonella collected within the EU harmonized antimicrobial resistance (AMR) surveillance programme in 2014–18 and the Danish AMR surveillance programme in 2016–19.

Methods

WGS data of 1007 E. coli [165 azithromycin resistant (MIC > 16 mg/L)] and 269 Salmonella [29 azithromycin resistant (MIC > 16 mg/L)] were screened for acquired macrolide resistance genes and mutations in rplDV, 23S rRNA and acrB genes using ResFinder v4.0, AMRFinder Plus and custom scripts. Genotype–phenotype concordance was determined for all isolates. Transferability of mef(C)-mph(G)-carrying plasmids was assessed by conjugation experiments.

Results

mph(A), mph(B), mef(B), erm(B) and mef(C)-mph(G) were detected in E. coli and Salmonella, whereas erm(C), erm(42), ere(A) and mph(E)-msr(E) were detected in E. coli only. The presence of macrolide resistance genes, alone or in combination, was concordant with the azithromycin-resistant phenotype in 69% of isolates. Distinct mph(A) operon structures were observed in azithromycin-susceptible (n = 50) and -resistant (n = 136) isolates. mef(C)-mph(G) were detected in porcine and bovine E. coli and in porcine Salmonella enterica serovar Derby and Salmonella enterica 1,4, [5],12:i:-, flanked downstream by ISCR2 or TnAs1 and associated with IncIγ and IncFII plasmids.

Conclusions

Diverse azithromycin resistance genes were detected in E. coli and Salmonella from food-producing animals and meat in Europe. Azithromycin resistance genes mef(C)-mph(G) and erm(42) appear to be emerging primarily in porcine E. coli isolates. The identification of distinct mph(A) operon structures in susceptible and resistant isolates increases the predictive power of WGS-based methods for in silico detection of azithromycin resistance in Enterobacterales.

Original language	English
Article number	dkae161
Journal	Journal of Antimicrobial Chemotherapy
Volume	79
Issue number	7
Pages (from-to)	1657-1667
Number of pages	11
ISSN	0305-7453
DOIs	https://doi.org/10.1093/jac/dkae161
Publication status	Published - 2024

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Ivanova, M., Ovsepian, A., Leekitcharoenphon, P., Seyfarth, A. M., Mordhorst, H., Otani, S., Koeberl-Jelovcan, S., Milanov, M., Kompes, G., Liapi, M., Černý, T., Vester, C. T., Perrin-Guyomard, A., Hammerl, J. A., Grobbel, M., Valkanou, E., Jánosi, S., Slowey, R., Alba, P., ... Kjeldgaard, J. S. (2024). Azithromycin resistance in Escherichia coli and Salmonella from food-producing animals and meat in Europe. Journal of Antimicrobial Chemotherapy, 79(7), 1657-1667. Article dkae161. https://doi.org/10.1093/jac/dkae161

@article{03abe1f3baf743059a65083abf2f4744,

title = "Azithromycin resistance in Escherichia coli and Salmonella from food-producing animals and meat in Europe",

abstract = "ObjectivesTo characterize the genetic basis of azithromycin resistance in Escherichia coli and Salmonella collected within the EU harmonized antimicrobial resistance (AMR) surveillance programme in 2014–18 and the Danish AMR surveillance programme in 2016–19.MethodsWGS data of 1007 E. coli [165 azithromycin resistant (MIC > 16 mg/L)] and 269 Salmonella [29 azithromycin resistant (MIC > 16 mg/L)] were screened for acquired macrolide resistance genes and mutations in rplDV, 23S rRNA and acrB genes using ResFinder v4.0, AMRFinder Plus and custom scripts. Genotype–phenotype concordance was determined for all isolates. Transferability of mef(C)-mph(G)-carrying plasmids was assessed by conjugation experiments.Resultsmph(A), mph(B), mef(B), erm(B) and mef(C)-mph(G) were detected in E. coli and Salmonella, whereas erm(C), erm(42), ere(A) and mph(E)-msr(E) were detected in E. coli only. The presence of macrolide resistance genes, alone or in combination, was concordant with the azithromycin-resistant phenotype in 69% of isolates. Distinct mph(A) operon structures were observed in azithromycin-susceptible (n = 50) and -resistant (n = 136) isolates. mef(C)-mph(G) were detected in porcine and bovine E. coli and in porcine Salmonella enterica serovar Derby and Salmonella enterica 1,4, [5],12:i:-, flanked downstream by ISCR2 or TnAs1 and associated with IncIγ and IncFII plasmids.ConclusionsDiverse azithromycin resistance genes were detected in E. coli and Salmonella from food-producing animals and meat in Europe. Azithromycin resistance genes mef(C)-mph(G) and erm(42) appear to be emerging primarily in porcine E. coli isolates. The identification of distinct mph(A) operon structures in susceptible and resistant isolates increases the predictive power of WGS-based methods for in silico detection of azithromycin resistance in Enterobacterales.",

author = "Mirena Ivanova and Armen Ovsepian and Pimlapas Leekitcharoenphon and Seyfarth, {Anne Mette} and Hanne Mordhorst and Saria Otani and Sandra Koeberl-Jelovcan and Mihail Milanov and Gordan Kompes and Maria Liapi and Tom{\'a}{\v s} {\v C}ern{\'y} and Vester, {Camilla Thougaard} and Agn{\`e}s Perrin-Guyomard and Hammerl, {Jens A} and Mirjam Grobbel and Eleni Valkanou and Szil{\'a}rd J{\'a}nosi and Rosemarie Slowey and Patricia Alba and Virginia Carfora and Jelena Avsejenko and Asta Pereckiene and Dominique Claude and Renato Zerafa and Veldman, {Kees T} and C{\'e}cile Boland and Cristina Garcia-Graells and Pierre Wattiau and Patrick Butaye and Magdalena Zaj{\c a}c and Ana Amaro and Lurdes Clemente and Vaduva, {Angela M} and Luminita-Maria Romascu and Nicoleta-Manuela Milita and Andrea Moj{\v z}i{\v s}ov{\'a} and Irena Zdovc and Escribano, {Maria Jes{\'u}s Zamora} and {De Frutos Escobar}, Cristina and Gudrun Overesch and Christopher Teale and Loneragan, {Guy H} and Beatriz Guerra and Beloeil, {Pierre Alexandre} and Brown, {Amanda M V} and Hendriksen, {Rene S} and Valeria Bortolaia and Kjeldgaard, {Jette Sejer}",

year = "2024",

doi = "10.1093/jac/dkae161",

language = "English",

volume = "79",

pages = "1657--1667",

journal = "Journal of Antimicrobial Chemotherapy",

issn = "0305-7453",

publisher = "Oxford University Press",

number = "7",

}

Ivanova, M, Ovsepian, A, Leekitcharoenphon, P, Seyfarth, AM, Mordhorst, H, Otani, S, Koeberl-Jelovcan, S, Milanov, M, Kompes, G, Liapi, M, Černý, T, Vester, CT, Perrin-Guyomard, A, Hammerl, JA, Grobbel, M, Valkanou, E, Jánosi, S, Slowey, R, Alba, P, Carfora, V, Avsejenko, J, Pereckiene, A, Claude, D, Zerafa, R, Veldman, KT, Boland, C, Garcia-Graells, C, Wattiau, P, Butaye, P, Zając, M, Amaro, A, Clemente, L, Vaduva, AM, Romascu, L-M, Milita, N-M, Mojžišová, A, Zdovc, I, Escribano, MJZ, De Frutos Escobar, C, Overesch, G, Teale, C, Loneragan, GH, Guerra, B, Beloeil, PA, Brown, AMV, Hendriksen, RS, Bortolaia, V & Kjeldgaard, JS 2024, 'Azithromycin resistance in Escherichia coli and Salmonella from food-producing animals and meat in Europe', Journal of Antimicrobial Chemotherapy, vol. 79, no. 7, dkae161, pp. 1657-1667. https://doi.org/10.1093/jac/dkae161

TY - JOUR

T1 - Azithromycin resistance in Escherichia coli and Salmonella from food-producing animals and meat in Europe

AU - Ivanova, Mirena

AU - Ovsepian, Armen

AU - Leekitcharoenphon, Pimlapas

AU - Seyfarth, Anne Mette

AU - Mordhorst, Hanne

AU - Otani, Saria

AU - Koeberl-Jelovcan, Sandra

AU - Milanov, Mihail

AU - Kompes, Gordan

AU - Liapi, Maria

AU - Černý, Tomáš

AU - Vester, Camilla Thougaard

AU - Perrin-Guyomard, Agnès

AU - Hammerl, Jens A

AU - Grobbel, Mirjam

AU - Valkanou, Eleni

AU - Jánosi, Szilárd

AU - Slowey, Rosemarie

AU - Alba, Patricia

AU - Carfora, Virginia

AU - Avsejenko, Jelena

AU - Pereckiene, Asta

AU - Claude, Dominique

AU - Zerafa, Renato

AU - Veldman, Kees T

AU - Boland, Cécile

AU - Garcia-Graells, Cristina

AU - Wattiau, Pierre

AU - Butaye, Patrick

AU - Zając, Magdalena

AU - Amaro, Ana

AU - Clemente, Lurdes

AU - Vaduva, Angela M

AU - Romascu, Luminita-Maria

AU - Milita, Nicoleta-Manuela

AU - Mojžišová, Andrea

AU - Zdovc, Irena

AU - Escribano, Maria Jesús Zamora

AU - De Frutos Escobar, Cristina

AU - Overesch, Gudrun

AU - Teale, Christopher

AU - Loneragan, Guy H

AU - Guerra, Beatriz

AU - Beloeil, Pierre Alexandre

AU - Brown, Amanda M V

AU - Hendriksen, Rene S

AU - Bortolaia, Valeria

AU - Kjeldgaard, Jette Sejer

PY - 2024

Y1 - 2024

N2 - ObjectivesTo characterize the genetic basis of azithromycin resistance in Escherichia coli and Salmonella collected within the EU harmonized antimicrobial resistance (AMR) surveillance programme in 2014–18 and the Danish AMR surveillance programme in 2016–19.MethodsWGS data of 1007 E. coli [165 azithromycin resistant (MIC > 16 mg/L)] and 269 Salmonella [29 azithromycin resistant (MIC > 16 mg/L)] were screened for acquired macrolide resistance genes and mutations in rplDV, 23S rRNA and acrB genes using ResFinder v4.0, AMRFinder Plus and custom scripts. Genotype–phenotype concordance was determined for all isolates. Transferability of mef(C)-mph(G)-carrying plasmids was assessed by conjugation experiments.Resultsmph(A), mph(B), mef(B), erm(B) and mef(C)-mph(G) were detected in E. coli and Salmonella, whereas erm(C), erm(42), ere(A) and mph(E)-msr(E) were detected in E. coli only. The presence of macrolide resistance genes, alone or in combination, was concordant with the azithromycin-resistant phenotype in 69% of isolates. Distinct mph(A) operon structures were observed in azithromycin-susceptible (n = 50) and -resistant (n = 136) isolates. mef(C)-mph(G) were detected in porcine and bovine E. coli and in porcine Salmonella enterica serovar Derby and Salmonella enterica 1,4, [5],12:i:-, flanked downstream by ISCR2 or TnAs1 and associated with IncIγ and IncFII plasmids.ConclusionsDiverse azithromycin resistance genes were detected in E. coli and Salmonella from food-producing animals and meat in Europe. Azithromycin resistance genes mef(C)-mph(G) and erm(42) appear to be emerging primarily in porcine E. coli isolates. The identification of distinct mph(A) operon structures in susceptible and resistant isolates increases the predictive power of WGS-based methods for in silico detection of azithromycin resistance in Enterobacterales.

AB - ObjectivesTo characterize the genetic basis of azithromycin resistance in Escherichia coli and Salmonella collected within the EU harmonized antimicrobial resistance (AMR) surveillance programme in 2014–18 and the Danish AMR surveillance programme in 2016–19.MethodsWGS data of 1007 E. coli [165 azithromycin resistant (MIC > 16 mg/L)] and 269 Salmonella [29 azithromycin resistant (MIC > 16 mg/L)] were screened for acquired macrolide resistance genes and mutations in rplDV, 23S rRNA and acrB genes using ResFinder v4.0, AMRFinder Plus and custom scripts. Genotype–phenotype concordance was determined for all isolates. Transferability of mef(C)-mph(G)-carrying plasmids was assessed by conjugation experiments.Resultsmph(A), mph(B), mef(B), erm(B) and mef(C)-mph(G) were detected in E. coli and Salmonella, whereas erm(C), erm(42), ere(A) and mph(E)-msr(E) were detected in E. coli only. The presence of macrolide resistance genes, alone or in combination, was concordant with the azithromycin-resistant phenotype in 69% of isolates. Distinct mph(A) operon structures were observed in azithromycin-susceptible (n = 50) and -resistant (n = 136) isolates. mef(C)-mph(G) were detected in porcine and bovine E. coli and in porcine Salmonella enterica serovar Derby and Salmonella enterica 1,4, [5],12:i:-, flanked downstream by ISCR2 or TnAs1 and associated with IncIγ and IncFII plasmids.ConclusionsDiverse azithromycin resistance genes were detected in E. coli and Salmonella from food-producing animals and meat in Europe. Azithromycin resistance genes mef(C)-mph(G) and erm(42) appear to be emerging primarily in porcine E. coli isolates. The identification of distinct mph(A) operon structures in susceptible and resistant isolates increases the predictive power of WGS-based methods for in silico detection of azithromycin resistance in Enterobacterales.

U2 - 10.1093/jac/dkae161

DO - 10.1093/jac/dkae161

M3 - Journal article

C2 - 38775752

SN - 0305-7453

VL - 79

SP - 1657

EP - 1667

JO - Journal of Antimicrobial Chemotherapy

JF - Journal of Antimicrobial Chemotherapy

IS - 7

M1 - dkae161

ER -

Azithromycin resistance in Escherichia coli and Salmonella from food-producing animals and meat in Europe

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