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

Jockey Club College of Veterinary Medicine and Life Sciences

Research output: Journal Publications and Reviews › RGC 21 - Publication in refereed journal › 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. © 2024 The Author(s).

Original language	English
Pages (from-to)	1657-1667
Journal	Journal of Antimicrobial Chemotherapy
Volume	79
Issue number	7
Online published	22 May 2024
DOIs	https://doi.org/10.1093/jac/dkae161
Publication status	Published - Jul 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. https://doi.org/10.1093/jac/dkae161

@article{df652e4b94604ca096c3467a0d229fca,

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

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. {\textcopyright} 2024 The Author(s).",

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",

month = jul,

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, 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 - 2024/7

Y1 - 2024/7

N2 - 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. © 2024 The Author(s).

AB - 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. © 2024 The Author(s).

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UR - https://www.scopus.com/record/pubmetrics.uri?eid=2-s2.0-85197962024&origin=recordpage

U2 - 10.1093/jac/dkae161

DO - 10.1093/jac/dkae161

M3 - RGC 21 - Publication in refereed journal

C2 - 38775752

SN - 0305-7453

VL - 79

SP - 1657

EP - 1667

JO - Journal of Antimicrobial Chemotherapy

JF - Journal of Antimicrobial Chemotherapy

IS - 7

ER -

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

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