Genetic Determinants of Resistance to Extended-Spectrum Cephalosporin and Fluoroquinolone in <named-content content-type="genus-species">Escherichia coli</named-content> Isolated from Diseased Pigs in the United States
ABSTRACT Fluoroquinolones and cephalosporins are critically important antimicrobial classes for both human and veterinary medicine. We previously found a drastic increase in enrofloxacin resistance in clinical Escherichia coli isolates collected from diseased pigs from the United States over 10 year...
Guardado en:
| Autores principales: | , , , , , , , , , |
|---|---|
| Formato: | article |
| Lenguaje: | EN |
| Publicado: |
American Society for Microbiology
2020
|
| Materias: | |
| Acceso en línea: | https://doaj.org/article/3e46822616704c94abc6a583c8c9e4e2 |
| Etiquetas: |
Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
|
| id |
oai:doaj.org-article:3e46822616704c94abc6a583c8c9e4e2 |
|---|---|
| record_format |
dspace |
| spelling |
oai:doaj.org-article:3e46822616704c94abc6a583c8c9e4e22021-11-15T15:30:59ZGenetic Determinants of Resistance to Extended-Spectrum Cephalosporin and Fluoroquinolone in <named-content content-type="genus-species">Escherichia coli</named-content> Isolated from Diseased Pigs in the United States10.1128/mSphere.00990-202379-5042https://doaj.org/article/3e46822616704c94abc6a583c8c9e4e22020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00990-20https://doaj.org/toc/2379-5042ABSTRACT Fluoroquinolones and cephalosporins are critically important antimicrobial classes for both human and veterinary medicine. We previously found a drastic increase in enrofloxacin resistance in clinical Escherichia coli isolates collected from diseased pigs from the United States over 10 years (2006 to 2016). However, the genetic determinants responsible for this increase have yet to be determined. The aim of the present study was to identify and characterize the genetic basis of resistance against fluoroquinolones (enrofloxacin) and extended-spectrum cephalosporins (ceftiofur) in swine E. coli isolates using whole-genome sequencing (WGS). blaCMY-2 (carried by IncA/C2, IncI1, and IncI2 plasmids), blaCTX-M (carried by IncF, IncHI2, and IncN plasmids), and blaSHV-12 (carried by IncHI2 plasmids) genes were present in 87 (82.1%), 19 (17.9%), and 3 (2.83%) of the 106 ceftiofur-resistant isolates, respectively. Of the 110 enrofloxacin-resistant isolates, 90 (81.8%) had chromosomal mutations in gyrA, gyrB, parA, and parC genes. Plasmid-mediated quinolone resistance genes [qnrB77, qnrB2, qnrS1, qnrS2, and aac-(6)-lb′-cr] borne on ColE, IncQ2, IncN, IncF, and IncHI2 plasmids were present in 24 (21.8%) of the enrofloxacin-resistant isolates. Virulent IncF plasmids present in swine E. coli isolates were highly similar to epidemic plasmids identified globally. High-risk E. coli clones, such as ST744, ST457, ST131, ST69, ST10, ST73, ST410, ST12, ST127, ST167, ST58, ST88, ST617, ST23, etc., were also found in the U.S. swine population. Additionally, the colistin resistance gene (mcr-9) was present in several isolates. This study adds valuable information regarding resistance to critical antimicrobials with implications for both animal and human health. IMPORTANCE Understanding the genetic mechanisms conferring resistance is critical to design informed control and preventive measures, particularly when involving critically important antimicrobial classes such as extended-spectrum cephalosporins and fluoroquinolones. The genetic determinants of extended-spectrum cephalosporin and fluoroquinolone resistance were highly diverse, with multiple plasmids, insertion sequences, and genes playing key roles in mediating resistance in swine Escherichia coli. Plasmids assembled in this study are known to be disseminated globally in both human and animal populations and environmental samples, and E. coli in pigs might be part of a global reservoir of key antimicrobial resistance (AMR) elements. Virulent plasmids found in this study have been shown to confer fitness advantages to pathogenic E. coli strains. The presence of international, high-risk zoonotic clones provides worrisome evidence that resistance in swine isolates may have indirect public health implications, and the swine population as a reservoir for these high-risk clones should be continuously monitored.Shivdeep Singh HayerSeunghyun LimSamuel HongEhud ElnekaveTimothy JohnsonAlbert RoviraFabio VannucciJonathan B. ClaytonAndres PerezJulio AlvarezAmerican Society for MicrobiologyarticleplasmidsESBLsswineUSAPMQRWGSMicrobiologyQR1-502ENmSphere, Vol 5, Iss 5 (2020) |
| institution |
DOAJ |
| collection |
DOAJ |
| language |
EN |
| topic |
plasmids ESBLs swine USA PMQR WGS Microbiology QR1-502 |
| spellingShingle |
plasmids ESBLs swine USA PMQR WGS Microbiology QR1-502 Shivdeep Singh Hayer Seunghyun Lim Samuel Hong Ehud Elnekave Timothy Johnson Albert Rovira Fabio Vannucci Jonathan B. Clayton Andres Perez Julio Alvarez Genetic Determinants of Resistance to Extended-Spectrum Cephalosporin and Fluoroquinolone in <named-content content-type="genus-species">Escherichia coli</named-content> Isolated from Diseased Pigs in the United States |
| description |
ABSTRACT Fluoroquinolones and cephalosporins are critically important antimicrobial classes for both human and veterinary medicine. We previously found a drastic increase in enrofloxacin resistance in clinical Escherichia coli isolates collected from diseased pigs from the United States over 10 years (2006 to 2016). However, the genetic determinants responsible for this increase have yet to be determined. The aim of the present study was to identify and characterize the genetic basis of resistance against fluoroquinolones (enrofloxacin) and extended-spectrum cephalosporins (ceftiofur) in swine E. coli isolates using whole-genome sequencing (WGS). blaCMY-2 (carried by IncA/C2, IncI1, and IncI2 plasmids), blaCTX-M (carried by IncF, IncHI2, and IncN plasmids), and blaSHV-12 (carried by IncHI2 plasmids) genes were present in 87 (82.1%), 19 (17.9%), and 3 (2.83%) of the 106 ceftiofur-resistant isolates, respectively. Of the 110 enrofloxacin-resistant isolates, 90 (81.8%) had chromosomal mutations in gyrA, gyrB, parA, and parC genes. Plasmid-mediated quinolone resistance genes [qnrB77, qnrB2, qnrS1, qnrS2, and aac-(6)-lb′-cr] borne on ColE, IncQ2, IncN, IncF, and IncHI2 plasmids were present in 24 (21.8%) of the enrofloxacin-resistant isolates. Virulent IncF plasmids present in swine E. coli isolates were highly similar to epidemic plasmids identified globally. High-risk E. coli clones, such as ST744, ST457, ST131, ST69, ST10, ST73, ST410, ST12, ST127, ST167, ST58, ST88, ST617, ST23, etc., were also found in the U.S. swine population. Additionally, the colistin resistance gene (mcr-9) was present in several isolates. This study adds valuable information regarding resistance to critical antimicrobials with implications for both animal and human health. IMPORTANCE Understanding the genetic mechanisms conferring resistance is critical to design informed control and preventive measures, particularly when involving critically important antimicrobial classes such as extended-spectrum cephalosporins and fluoroquinolones. The genetic determinants of extended-spectrum cephalosporin and fluoroquinolone resistance were highly diverse, with multiple plasmids, insertion sequences, and genes playing key roles in mediating resistance in swine Escherichia coli. Plasmids assembled in this study are known to be disseminated globally in both human and animal populations and environmental samples, and E. coli in pigs might be part of a global reservoir of key antimicrobial resistance (AMR) elements. Virulent plasmids found in this study have been shown to confer fitness advantages to pathogenic E. coli strains. The presence of international, high-risk zoonotic clones provides worrisome evidence that resistance in swine isolates may have indirect public health implications, and the swine population as a reservoir for these high-risk clones should be continuously monitored. |
| format |
article |
| author |
Shivdeep Singh Hayer Seunghyun Lim Samuel Hong Ehud Elnekave Timothy Johnson Albert Rovira Fabio Vannucci Jonathan B. Clayton Andres Perez Julio Alvarez |
| author_facet |
Shivdeep Singh Hayer Seunghyun Lim Samuel Hong Ehud Elnekave Timothy Johnson Albert Rovira Fabio Vannucci Jonathan B. Clayton Andres Perez Julio Alvarez |
| author_sort |
Shivdeep Singh Hayer |
| title |
Genetic Determinants of Resistance to Extended-Spectrum Cephalosporin and Fluoroquinolone in <named-content content-type="genus-species">Escherichia coli</named-content> Isolated from Diseased Pigs in the United States |
| title_short |
Genetic Determinants of Resistance to Extended-Spectrum Cephalosporin and Fluoroquinolone in <named-content content-type="genus-species">Escherichia coli</named-content> Isolated from Diseased Pigs in the United States |
| title_full |
Genetic Determinants of Resistance to Extended-Spectrum Cephalosporin and Fluoroquinolone in <named-content content-type="genus-species">Escherichia coli</named-content> Isolated from Diseased Pigs in the United States |
| title_fullStr |
Genetic Determinants of Resistance to Extended-Spectrum Cephalosporin and Fluoroquinolone in <named-content content-type="genus-species">Escherichia coli</named-content> Isolated from Diseased Pigs in the United States |
| title_full_unstemmed |
Genetic Determinants of Resistance to Extended-Spectrum Cephalosporin and Fluoroquinolone in <named-content content-type="genus-species">Escherichia coli</named-content> Isolated from Diseased Pigs in the United States |
| title_sort |
genetic determinants of resistance to extended-spectrum cephalosporin and fluoroquinolone in <named-content content-type="genus-species">escherichia coli</named-content> isolated from diseased pigs in the united states |
| publisher |
American Society for Microbiology |
| publishDate |
2020 |
| url |
https://doaj.org/article/3e46822616704c94abc6a583c8c9e4e2 |
| work_keys_str_mv |
AT shivdeepsinghhayer geneticdeterminantsofresistancetoextendedspectrumcephalosporinandfluoroquinoloneinnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentisolatedfromdiseasedpigsintheunitedstates AT seunghyunlim geneticdeterminantsofresistancetoextendedspectrumcephalosporinandfluoroquinoloneinnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentisolatedfromdiseasedpigsintheunitedstates AT samuelhong geneticdeterminantsofresistancetoextendedspectrumcephalosporinandfluoroquinoloneinnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentisolatedfromdiseasedpigsintheunitedstates AT ehudelnekave geneticdeterminantsofresistancetoextendedspectrumcephalosporinandfluoroquinoloneinnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentisolatedfromdiseasedpigsintheunitedstates AT timothyjohnson geneticdeterminantsofresistancetoextendedspectrumcephalosporinandfluoroquinoloneinnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentisolatedfromdiseasedpigsintheunitedstates AT albertrovira geneticdeterminantsofresistancetoextendedspectrumcephalosporinandfluoroquinoloneinnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentisolatedfromdiseasedpigsintheunitedstates AT fabiovannucci geneticdeterminantsofresistancetoextendedspectrumcephalosporinandfluoroquinoloneinnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentisolatedfromdiseasedpigsintheunitedstates AT jonathanbclayton geneticdeterminantsofresistancetoextendedspectrumcephalosporinandfluoroquinoloneinnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentisolatedfromdiseasedpigsintheunitedstates AT andresperez geneticdeterminantsofresistancetoextendedspectrumcephalosporinandfluoroquinoloneinnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentisolatedfromdiseasedpigsintheunitedstates AT julioalvarez geneticdeterminantsofresistancetoextendedspectrumcephalosporinandfluoroquinoloneinnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentisolatedfromdiseasedpigsintheunitedstates |
| _version_ |
1718427820485509120 |