Abrupt emergence of a single dominant multidrug-resistant strain of Escherichia coli

James R. Johnson; Veronika Tchesnokova; Brian Johnston; Connie Clabots; Pacita L. Roberts; Mariya Billig; Kim Riddell; Peggy Rogers; Xuan Qin; Susan Butler-Wu; Lance B. Price; Maliha Aziz; Marie Hélène Nicolas-Chanoine; Chitrita Debroy; Ari Robicsek; Glen Hansen; Carl Urban; Joanne Platell; Darren J. Trott; George Zhanel; Scott J. Weissman; Brad T. Cookson; Ferric C. Fang; Ajit P. Limaye; Delia Scholes; Sujay Chattopadhyay; David C. Hooper; Evgeni V. Sokurenko

doi:10.1093/infdis/jis933

Abrupt emergence of a single dominant multidrug-resistant strain of Escherichia coli

James R. Johnson, Veronika Tchesnokova, Brian Johnston, Connie Clabots, Pacita L. Roberts, Mariya Billig, Kim Riddell, Peggy Rogers, Xuan Qin, Susan Butler-Wu, Lance B. Price, Maliha Aziz, Marie Hélène Nicolas-Chanoine, Chitrita Debroy, Ari Robicsek, Glen Hansen, Carl Urban, Joanne Platell, Darren J. Trott, George ZhanelScott J. Weissman, Brad T. Cookson, Ferric C. Fang, Ajit P. Limaye, Delia Scholes, Sujay Chattopadhyay, David C. Hooper, Evgeni V. Sokurenko

Medicine - Veteran's Administration Medical Center

Research output: Contribution to journal › Article › peer-review

215 Scopus citations

Abstract

Background. Fluoroquinolone-resistant Escherichia coli are increasingly prevalent. Their clonal origins-potentially critical for control efforts-remain undefined.Methods. Antimicrobial resistance profiles and fine clonal structure were determined for 236 diverse-source historical (1967-2009) E. coli isolates representing sequence type ST131 and 853 recent (2010-2011) consecutive E. coli isolates from 5 clinical laboratories in Seattle, Washington, and Minneapolis, Minnesota. Clonal structure was resolved based on fimH sequence (fimbrial adhesin gene: H subclone assignments), multilocus sequence typing, gyrA and parC sequence (fluoroquinolone resistance-determining loci), and pulsed-field gel electrophoresis.Results. Of the recent fluoroquinolone-resistant clinical isolates, 52% represented a single ST131 subclonal lineage, H30, which expanded abruptly after 2000. This subclone had a unique and conserved gyrA/parC allele combination, supporting its tight clonality. Unlike other ST131 subclones, H30 was significantly associated with fluoroquinolone resistance and was the most prevalent subclone among current E. coli clinical isolates, overall (10.4%) and within every resistance category (11%-52%).Conclusions. Most current fluoroquinolone-resistant E. coli clinical isolates, and the largest share of multidrug-resistant isolates, represent a highly clonal subgroup that likely originated from a single rapidly expanded and disseminated ST131 strain. Focused attention to this strain will be required to control the fluoroquinolone and multidrug-resistant E. coli epidemic.

Original language	English (US)
Pages (from-to)	919-928
Number of pages	10
Journal	Journal of Infectious Diseases
Volume	207
Issue number	6
DOIs	https://doi.org/10.1093/infdis/jis933
State	Published - 2013

Bibliographical note

Funding Information:
Potential conflicts of interest. The following authors report these conflicts of interest: F. C. F.: Consultancy, research grants, and educational presentations with Cepheid. D. C. H.: Research grant from Rib-X Pharmaceuticals, consultancies with Fab Pharma and Pfizer, speakers bureau with Pfizer. J. R. J.: Research grants and contracts from Merck, Rochester Medical, and Syntiron; patent pending for detection of the H30 ST131 subclone. L. B. P.: Patent pending for detection of the H30 ST131 subclone. M.-H. N.-C.: Expert testimony for Region Wallon; research grant from Direction de la Recherche Clinique AP-HP; lectures for Novar-tis; travel reimbursement for 2012 ICAAC speaker. E. V. S.: Research grant from Group Health; patent pending for detection of the H30 ST131 subclone. D. T.: Research grant from ARC Linkage; consultancy from Pfizer and Bayer; speaker for Bayer Animal Health. C. U.: Consultancy with Pfizer, lecture/speaker for Forest Pharmaceuticals, Cubist, and Pfizer. G. Z.: Research grants from Achaogen, Merck, Pfizer, Cubist, Affi-nium, and Sunovion. All other authors report no potential conflicts.

Funding Information:
Financial support. This material is based upon work supported by Office of Research and Development, Medical Research Service, Department of Veterans Affairs, Merit Review grant 1 I01 CX000192 01 ( J. R. J.), and NIH ARRA award 1RC4AI092828 (E. V. S.).

Keywords

CTX-M-15
Escherichia coli infections
FimH
antimicrobial resistance
extended-spectrum β-lactamase
fluoroquinolone resistance
molecular epidemiology
multidrug resistance
multilocus sequence typing
sequence type ST131

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Johnson, J. R., Tchesnokova, V., Johnston, B., Clabots, C., Roberts, P. L., Billig, M., Riddell, K., Rogers, P., Qin, X., Butler-Wu, S., Price, L. B., Aziz, M., Nicolas-Chanoine, M. H., Debroy, C., Robicsek, A., Hansen, G., Urban, C., Platell, J., Trott, D. J., ... Sokurenko, E. V. (2013). Abrupt emergence of a single dominant multidrug-resistant strain of Escherichia coli. Journal of Infectious Diseases, 207(6), 919-928. https://doi.org/10.1093/infdis/jis933

Johnson, JR, Tchesnokova, V, Johnston, B, Clabots, C, Roberts, PL, Billig, M, Riddell, K, Rogers, P, Qin, X, Butler-Wu, S, Price, LB, Aziz, M, Nicolas-Chanoine, MH, Debroy, C, Robicsek, A, Hansen, G, Urban, C, Platell, J, Trott, DJ, Zhanel, G, Weissman, SJ, Cookson, BT, Fang, FC, Limaye, AP, Scholes, D, Chattopadhyay, S, Hooper, DC & Sokurenko, EV 2013, 'Abrupt emergence of a single dominant multidrug-resistant strain of Escherichia coli', Journal of Infectious Diseases, vol. 207, no. 6, pp. 919-928. https://doi.org/10.1093/infdis/jis933

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title = "Abrupt emergence of a single dominant multidrug-resistant strain of Escherichia coli",

abstract = "Background. Fluoroquinolone-resistant Escherichia coli are increasingly prevalent. Their clonal origins-potentially critical for control efforts-remain undefined.Methods. Antimicrobial resistance profiles and fine clonal structure were determined for 236 diverse-source historical (1967-2009) E. coli isolates representing sequence type ST131 and 853 recent (2010-2011) consecutive E. coli isolates from 5 clinical laboratories in Seattle, Washington, and Minneapolis, Minnesota. Clonal structure was resolved based on fimH sequence (fimbrial adhesin gene: H subclone assignments), multilocus sequence typing, gyrA and parC sequence (fluoroquinolone resistance-determining loci), and pulsed-field gel electrophoresis.Results. Of the recent fluoroquinolone-resistant clinical isolates, 52% represented a single ST131 subclonal lineage, H30, which expanded abruptly after 2000. This subclone had a unique and conserved gyrA/parC allele combination, supporting its tight clonality. Unlike other ST131 subclones, H30 was significantly associated with fluoroquinolone resistance and was the most prevalent subclone among current E. coli clinical isolates, overall (10.4%) and within every resistance category (11%-52%).Conclusions. Most current fluoroquinolone-resistant E. coli clinical isolates, and the largest share of multidrug-resistant isolates, represent a highly clonal subgroup that likely originated from a single rapidly expanded and disseminated ST131 strain. Focused attention to this strain will be required to control the fluoroquinolone and multidrug-resistant E. coli epidemic.",

keywords = "CTX-M-15, Escherichia coli infections, FimH, antimicrobial resistance, extended-spectrum β-lactamase, fluoroquinolone resistance, molecular epidemiology, multidrug resistance, multilocus sequence typing, sequence type ST131",

author = "Johnson, {James R.} and Veronika Tchesnokova and Brian Johnston and Connie Clabots and Roberts, {Pacita L.} and Mariya Billig and Kim Riddell and Peggy Rogers and Xuan Qin and Susan Butler-Wu and Price, {Lance B.} and Maliha Aziz and Nicolas-Chanoine, {Marie H{\'e}l{\`e}ne} and Chitrita Debroy and Ari Robicsek and Glen Hansen and Carl Urban and Joanne Platell and Trott, {Darren J.} and George Zhanel and Weissman, {Scott J.} and Cookson, {Brad T.} and Fang, {Ferric C.} and Limaye, {Ajit P.} and Delia Scholes and Sujay Chattopadhyay and Hooper, {David C.} and Sokurenko, {Evgeni V.}",

note = "Funding Information: Potential conflicts of interest. The following authors report these conflicts of interest: F. C. F.: Consultancy, research grants, and educational presentations with Cepheid. D. C. H.: Research grant from Rib-X Pharmaceuticals, consultancies with Fab Pharma and Pfizer, speakers bureau with Pfizer. J. R. J.: Research grants and contracts from Merck, Rochester Medical, and Syntiron; patent pending for detection of the H30 ST131 subclone. L. B. P.: Patent pending for detection of the H30 ST131 subclone. M.-H. N.-C.: Expert testimony for Region Wallon; research grant from Direction de la Recherche Clinique AP-HP; lectures for Novar-tis; travel reimbursement for 2012 ICAAC speaker. E. V. S.: Research grant from Group Health; patent pending for detection of the H30 ST131 subclone. D. T.: Research grant from ARC Linkage; consultancy from Pfizer and Bayer; speaker for Bayer Animal Health. C. U.: Consultancy with Pfizer, lecture/speaker for Forest Pharmaceuticals, Cubist, and Pfizer. G. Z.: Research grants from Achaogen, Merck, Pfizer, Cubist, Affi-nium, and Sunovion. All other authors report no potential conflicts. Funding Information: Financial support. This material is based upon work supported by Office of Research and Development, Medical Research Service, Department of Veterans Affairs, Merit Review grant 1 I01 CX000192 01 ( J. R. J.), and NIH ARRA award 1RC4AI092828 (E. V. S.).",

year = "2013",

doi = "10.1093/infdis/jis933",

language = "English (US)",

volume = "207",

pages = "919--928",

journal = "Journal of Infectious Diseases",

issn = "0022-1899",

publisher = "Oxford University Press",

number = "6",

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TY - JOUR

T1 - Abrupt emergence of a single dominant multidrug-resistant strain of Escherichia coli

AU - Johnson, James R.

AU - Tchesnokova, Veronika

AU - Johnston, Brian

AU - Clabots, Connie

AU - Roberts, Pacita L.

AU - Billig, Mariya

AU - Riddell, Kim

AU - Rogers, Peggy

AU - Qin, Xuan

AU - Butler-Wu, Susan

AU - Price, Lance B.

AU - Aziz, Maliha

AU - Nicolas-Chanoine, Marie Hélène

AU - Debroy, Chitrita

AU - Robicsek, Ari

AU - Hansen, Glen

AU - Urban, Carl

AU - Platell, Joanne

AU - Trott, Darren J.

AU - Zhanel, George

AU - Weissman, Scott J.

AU - Cookson, Brad T.

AU - Fang, Ferric C.

AU - Limaye, Ajit P.

AU - Scholes, Delia

AU - Chattopadhyay, Sujay

AU - Hooper, David C.

AU - Sokurenko, Evgeni V.

N1 - Funding Information: Potential conflicts of interest. The following authors report these conflicts of interest: F. C. F.: Consultancy, research grants, and educational presentations with Cepheid. D. C. H.: Research grant from Rib-X Pharmaceuticals, consultancies with Fab Pharma and Pfizer, speakers bureau with Pfizer. J. R. J.: Research grants and contracts from Merck, Rochester Medical, and Syntiron; patent pending for detection of the H30 ST131 subclone. L. B. P.: Patent pending for detection of the H30 ST131 subclone. M.-H. N.-C.: Expert testimony for Region Wallon; research grant from Direction de la Recherche Clinique AP-HP; lectures for Novar-tis; travel reimbursement for 2012 ICAAC speaker. E. V. S.: Research grant from Group Health; patent pending for detection of the H30 ST131 subclone. D. T.: Research grant from ARC Linkage; consultancy from Pfizer and Bayer; speaker for Bayer Animal Health. C. U.: Consultancy with Pfizer, lecture/speaker for Forest Pharmaceuticals, Cubist, and Pfizer. G. Z.: Research grants from Achaogen, Merck, Pfizer, Cubist, Affi-nium, and Sunovion. All other authors report no potential conflicts. Funding Information: Financial support. This material is based upon work supported by Office of Research and Development, Medical Research Service, Department of Veterans Affairs, Merit Review grant 1 I01 CX000192 01 ( J. R. J.), and NIH ARRA award 1RC4AI092828 (E. V. S.).

PY - 2013

Y1 - 2013

N2 - Background. Fluoroquinolone-resistant Escherichia coli are increasingly prevalent. Their clonal origins-potentially critical for control efforts-remain undefined.Methods. Antimicrobial resistance profiles and fine clonal structure were determined for 236 diverse-source historical (1967-2009) E. coli isolates representing sequence type ST131 and 853 recent (2010-2011) consecutive E. coli isolates from 5 clinical laboratories in Seattle, Washington, and Minneapolis, Minnesota. Clonal structure was resolved based on fimH sequence (fimbrial adhesin gene: H subclone assignments), multilocus sequence typing, gyrA and parC sequence (fluoroquinolone resistance-determining loci), and pulsed-field gel electrophoresis.Results. Of the recent fluoroquinolone-resistant clinical isolates, 52% represented a single ST131 subclonal lineage, H30, which expanded abruptly after 2000. This subclone had a unique and conserved gyrA/parC allele combination, supporting its tight clonality. Unlike other ST131 subclones, H30 was significantly associated with fluoroquinolone resistance and was the most prevalent subclone among current E. coli clinical isolates, overall (10.4%) and within every resistance category (11%-52%).Conclusions. Most current fluoroquinolone-resistant E. coli clinical isolates, and the largest share of multidrug-resistant isolates, represent a highly clonal subgroup that likely originated from a single rapidly expanded and disseminated ST131 strain. Focused attention to this strain will be required to control the fluoroquinolone and multidrug-resistant E. coli epidemic.

AB - Background. Fluoroquinolone-resistant Escherichia coli are increasingly prevalent. Their clonal origins-potentially critical for control efforts-remain undefined.Methods. Antimicrobial resistance profiles and fine clonal structure were determined for 236 diverse-source historical (1967-2009) E. coli isolates representing sequence type ST131 and 853 recent (2010-2011) consecutive E. coli isolates from 5 clinical laboratories in Seattle, Washington, and Minneapolis, Minnesota. Clonal structure was resolved based on fimH sequence (fimbrial adhesin gene: H subclone assignments), multilocus sequence typing, gyrA and parC sequence (fluoroquinolone resistance-determining loci), and pulsed-field gel electrophoresis.Results. Of the recent fluoroquinolone-resistant clinical isolates, 52% represented a single ST131 subclonal lineage, H30, which expanded abruptly after 2000. This subclone had a unique and conserved gyrA/parC allele combination, supporting its tight clonality. Unlike other ST131 subclones, H30 was significantly associated with fluoroquinolone resistance and was the most prevalent subclone among current E. coli clinical isolates, overall (10.4%) and within every resistance category (11%-52%).Conclusions. Most current fluoroquinolone-resistant E. coli clinical isolates, and the largest share of multidrug-resistant isolates, represent a highly clonal subgroup that likely originated from a single rapidly expanded and disseminated ST131 strain. Focused attention to this strain will be required to control the fluoroquinolone and multidrug-resistant E. coli epidemic.

KW - CTX-M-15

KW - Escherichia coli infections

KW - FimH

KW - antimicrobial resistance

KW - extended-spectrum β-lactamase

KW - fluoroquinolone resistance

KW - molecular epidemiology

KW - multidrug resistance

KW - multilocus sequence typing

KW - sequence type ST131

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U2 - 10.1093/infdis/jis933

DO - 10.1093/infdis/jis933

M3 - Article

C2 - 23288927

AN - SCOPUS:84874263817

SN - 0022-1899

VL - 207

SP - 919

EP - 928

JO - Journal of Infectious Diseases

JF - Journal of Infectious Diseases

IS - 6

ER -

Abrupt emergence of a single dominant multidrug-resistant strain of Escherichia coli

Abstract

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Keywords

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