Effect of outpatient antibiotics for urinary tract infections on antimicrobial resistance among commensal Enterobacteriaceae

A multinational prospective cohort study

A. J. Stewardson, J. Vervoort, N. Adriaenssens, S. Coenen, M. Godycki-Cwirko, A. Kowalczyk, B. D. Huttner, C. Lammens, S. Malhotra-Kumar, H. Goossens, S. Harbarth, on behalf of SATURN WP1 Study Group, SATURN WP3 Study Group

Research output: Contribution to journalArticleResearchpeer-review

Abstract

Objectives: We quantified the impact of antibiotics prescribed in primary care for urinary tract infections (UTIs) on intestinal colonization by ciprofloxacin-resistant (CIP-RE) and extended-spectrum β-lactamase-producing Enterobacteriaceae (ESBL-PE), while accounting for household clustering. Methods: Prospective cohort study from January 2011 to August 2013 at primary care sites in Belgium, Poland and Switzerland. We recruited outpatients requiring antibiotics for suspected UTIs or asymptomatic bacteriuria (exposed patients), outpatients not requiring antibiotics (non-exposed patients), and one to three household contacts for each patient. Faecal samples were tested for CIP-RE, ESBL-PE, nitrofurantoin-resistant Enterobacteriaceae (NIT-RE) and any Enterobacteriaceae at baseline (S1), end of antibiotics (S2) and 28 days after S2 (S3). Results: We included 300 households (205 exposed, 95 non-exposed) with 716 participants. Most exposed patients received nitrofurans (86; 42%) or fluoroquinolones (76; 37%). CIP-RE were identified in 16% (328/2033) of samples from 202 (28%) participants. Fluoroquinolone treatment caused transient suppression of Enterobacteriaceae (S2) and subsequent two-fold increase in CIP-RE prevalence at S3 (adjusted prevalence ratio (aPR) 2.0, 95% CI 1.2-3.4), with corresponding number-needed-to-harm of 12. Nitrofurans had no impact on CIP-RE (aPR 1.0, 95% CI 0.5-1.8) or NIT-RE. ESBL-PE were identified in 5% (107/2058) of samples from 71 (10%) participants, with colonization not associated with antibiotic exposure. Household exposure to CIP-RE or ESBL-PE was associated with increased individual risk of colonization: aPR 1.8 (95% CI 1.3-2.5) and 3.4 (95% CI 1.3-9.0), respectively. Conclusions: These findings support avoidance of fluoroquinolones for first-line UTI therapy in primary care, and suggest potential for interventions that interrupt household circulation of resistant Enterobacteriaceae.

Original languageEnglish
Pages (from-to)972–979
Number of pages8
JournalClinical Microbiology and Infection
Volume24
Issue number9
DOIs
Publication statusPublished - Sep 2018

Keywords

  • Antimicrobial resistance
  • Collateral damage
  • Enterobacteriaceae
  • Extended-spectrum β-lactamase
  • Fluoroquinolone
  • Microbiota
  • Nitrofuran
  • Urinary tract infection

Cite this

Stewardson, A. J. ; Vervoort, J. ; Adriaenssens, N. ; Coenen, S. ; Godycki-Cwirko, M. ; Kowalczyk, A. ; Huttner, B. D. ; Lammens, C. ; Malhotra-Kumar, S. ; Goossens, H. ; Harbarth, S. ; on behalf of SATURN WP1 Study Group ; SATURN WP3 Study Group. / Effect of outpatient antibiotics for urinary tract infections on antimicrobial resistance among commensal Enterobacteriaceae : A multinational prospective cohort study. In: Clinical Microbiology and Infection. 2018 ; Vol. 24, No. 9. pp. 972–979.
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title = "Effect of outpatient antibiotics for urinary tract infections on antimicrobial resistance among commensal Enterobacteriaceae: A multinational prospective cohort study",
abstract = "Objectives: We quantified the impact of antibiotics prescribed in primary care for urinary tract infections (UTIs) on intestinal colonization by ciprofloxacin-resistant (CIP-RE) and extended-spectrum β-lactamase-producing Enterobacteriaceae (ESBL-PE), while accounting for household clustering. Methods: Prospective cohort study from January 2011 to August 2013 at primary care sites in Belgium, Poland and Switzerland. We recruited outpatients requiring antibiotics for suspected UTIs or asymptomatic bacteriuria (exposed patients), outpatients not requiring antibiotics (non-exposed patients), and one to three household contacts for each patient. Faecal samples were tested for CIP-RE, ESBL-PE, nitrofurantoin-resistant Enterobacteriaceae (NIT-RE) and any Enterobacteriaceae at baseline (S1), end of antibiotics (S2) and 28 days after S2 (S3). Results: We included 300 households (205 exposed, 95 non-exposed) with 716 participants. Most exposed patients received nitrofurans (86; 42{\%}) or fluoroquinolones (76; 37{\%}). CIP-RE were identified in 16{\%} (328/2033) of samples from 202 (28{\%}) participants. Fluoroquinolone treatment caused transient suppression of Enterobacteriaceae (S2) and subsequent two-fold increase in CIP-RE prevalence at S3 (adjusted prevalence ratio (aPR) 2.0, 95{\%} CI 1.2-3.4), with corresponding number-needed-to-harm of 12. Nitrofurans had no impact on CIP-RE (aPR 1.0, 95{\%} CI 0.5-1.8) or NIT-RE. ESBL-PE were identified in 5{\%} (107/2058) of samples from 71 (10{\%}) participants, with colonization not associated with antibiotic exposure. Household exposure to CIP-RE or ESBL-PE was associated with increased individual risk of colonization: aPR 1.8 (95{\%} CI 1.3-2.5) and 3.4 (95{\%} CI 1.3-9.0), respectively. Conclusions: These findings support avoidance of fluoroquinolones for first-line UTI therapy in primary care, and suggest potential for interventions that interrupt household circulation of resistant Enterobacteriaceae.",
keywords = "Antimicrobial resistance, Collateral damage, Enterobacteriaceae, Extended-spectrum β-lactamase, Fluoroquinolone, Microbiota, Nitrofuran, Urinary tract infection",
author = "Stewardson, {A. J.} and J. Vervoort and N. Adriaenssens and S. Coenen and M. Godycki-Cwirko and A. Kowalczyk and Huttner, {B. D.} and C. Lammens and S. Malhotra-Kumar and H. Goossens and S. Harbarth and {on behalf of SATURN WP1 Study Group} and {SATURN WP3 Study Group}",
year = "2018",
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doi = "10.1016/j.cmi.2017.12.026",
language = "English",
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pages = "972–979",
journal = "Clinical Microbiology and Infection",
issn = "1198-743X",
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}

Stewardson, AJ, Vervoort, J, Adriaenssens, N, Coenen, S, Godycki-Cwirko, M, Kowalczyk, A, Huttner, BD, Lammens, C, Malhotra-Kumar, S, Goossens, H, Harbarth, S, on behalf of SATURN WP1 Study Group & SATURN WP3 Study Group 2018, 'Effect of outpatient antibiotics for urinary tract infections on antimicrobial resistance among commensal Enterobacteriaceae: A multinational prospective cohort study', Clinical Microbiology and Infection, vol. 24, no. 9, pp. 972–979. https://doi.org/10.1016/j.cmi.2017.12.026

Effect of outpatient antibiotics for urinary tract infections on antimicrobial resistance among commensal Enterobacteriaceae : A multinational prospective cohort study. / Stewardson, A. J.; Vervoort, J.; Adriaenssens, N.; Coenen, S.; Godycki-Cwirko, M.; Kowalczyk, A.; Huttner, B. D.; Lammens, C.; Malhotra-Kumar, S.; Goossens, H.; Harbarth, S.; on behalf of SATURN WP1 Study Group; SATURN WP3 Study Group.

In: Clinical Microbiology and Infection, Vol. 24, No. 9, 09.2018, p. 972–979.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Effect of outpatient antibiotics for urinary tract infections on antimicrobial resistance among commensal Enterobacteriaceae

T2 - A multinational prospective cohort study

AU - Stewardson, A. J.

AU - Vervoort, J.

AU - Adriaenssens, N.

AU - Coenen, S.

AU - Godycki-Cwirko, M.

AU - Kowalczyk, A.

AU - Huttner, B. D.

AU - Lammens, C.

AU - Malhotra-Kumar, S.

AU - Goossens, H.

AU - Harbarth, S.

AU - on behalf of SATURN WP1 Study Group

AU - SATURN WP3 Study Group

PY - 2018/9

Y1 - 2018/9

N2 - Objectives: We quantified the impact of antibiotics prescribed in primary care for urinary tract infections (UTIs) on intestinal colonization by ciprofloxacin-resistant (CIP-RE) and extended-spectrum β-lactamase-producing Enterobacteriaceae (ESBL-PE), while accounting for household clustering. Methods: Prospective cohort study from January 2011 to August 2013 at primary care sites in Belgium, Poland and Switzerland. We recruited outpatients requiring antibiotics for suspected UTIs or asymptomatic bacteriuria (exposed patients), outpatients not requiring antibiotics (non-exposed patients), and one to three household contacts for each patient. Faecal samples were tested for CIP-RE, ESBL-PE, nitrofurantoin-resistant Enterobacteriaceae (NIT-RE) and any Enterobacteriaceae at baseline (S1), end of antibiotics (S2) and 28 days after S2 (S3). Results: We included 300 households (205 exposed, 95 non-exposed) with 716 participants. Most exposed patients received nitrofurans (86; 42%) or fluoroquinolones (76; 37%). CIP-RE were identified in 16% (328/2033) of samples from 202 (28%) participants. Fluoroquinolone treatment caused transient suppression of Enterobacteriaceae (S2) and subsequent two-fold increase in CIP-RE prevalence at S3 (adjusted prevalence ratio (aPR) 2.0, 95% CI 1.2-3.4), with corresponding number-needed-to-harm of 12. Nitrofurans had no impact on CIP-RE (aPR 1.0, 95% CI 0.5-1.8) or NIT-RE. ESBL-PE were identified in 5% (107/2058) of samples from 71 (10%) participants, with colonization not associated with antibiotic exposure. Household exposure to CIP-RE or ESBL-PE was associated with increased individual risk of colonization: aPR 1.8 (95% CI 1.3-2.5) and 3.4 (95% CI 1.3-9.0), respectively. Conclusions: These findings support avoidance of fluoroquinolones for first-line UTI therapy in primary care, and suggest potential for interventions that interrupt household circulation of resistant Enterobacteriaceae.

AB - Objectives: We quantified the impact of antibiotics prescribed in primary care for urinary tract infections (UTIs) on intestinal colonization by ciprofloxacin-resistant (CIP-RE) and extended-spectrum β-lactamase-producing Enterobacteriaceae (ESBL-PE), while accounting for household clustering. Methods: Prospective cohort study from January 2011 to August 2013 at primary care sites in Belgium, Poland and Switzerland. We recruited outpatients requiring antibiotics for suspected UTIs or asymptomatic bacteriuria (exposed patients), outpatients not requiring antibiotics (non-exposed patients), and one to three household contacts for each patient. Faecal samples were tested for CIP-RE, ESBL-PE, nitrofurantoin-resistant Enterobacteriaceae (NIT-RE) and any Enterobacteriaceae at baseline (S1), end of antibiotics (S2) and 28 days after S2 (S3). Results: We included 300 households (205 exposed, 95 non-exposed) with 716 participants. Most exposed patients received nitrofurans (86; 42%) or fluoroquinolones (76; 37%). CIP-RE were identified in 16% (328/2033) of samples from 202 (28%) participants. Fluoroquinolone treatment caused transient suppression of Enterobacteriaceae (S2) and subsequent two-fold increase in CIP-RE prevalence at S3 (adjusted prevalence ratio (aPR) 2.0, 95% CI 1.2-3.4), with corresponding number-needed-to-harm of 12. Nitrofurans had no impact on CIP-RE (aPR 1.0, 95% CI 0.5-1.8) or NIT-RE. ESBL-PE were identified in 5% (107/2058) of samples from 71 (10%) participants, with colonization not associated with antibiotic exposure. Household exposure to CIP-RE or ESBL-PE was associated with increased individual risk of colonization: aPR 1.8 (95% CI 1.3-2.5) and 3.4 (95% CI 1.3-9.0), respectively. Conclusions: These findings support avoidance of fluoroquinolones for first-line UTI therapy in primary care, and suggest potential for interventions that interrupt household circulation of resistant Enterobacteriaceae.

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KW - Collateral damage

KW - Enterobacteriaceae

KW - Extended-spectrum β-lactamase

KW - Fluoroquinolone

KW - Microbiota

KW - Nitrofuran

KW - Urinary tract infection

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