Gastric acid suppression, lifestyle factors and intestinal carriage of ESBL and carbapenemase-producing Enterobacterales: a nationwide population-based study

Roel P.J. Willems; Karin van Dijk; Cindy M. Dierikx; Jos W.R. Twisk; Fiona R.M. van der Klis; Sabine C. de Greeff; Christina M.J.E. Vandenbroucke-Grauls

doi:10.1093/jac/dkab345

Gastric acid suppression, lifestyle factors and intestinal carriage of ESBL and carbapenemase-producing Enterobacterales: a nationwide population-based study

Roel P.J. Willems, Karin van Dijk, Cindy M. Dierikx, Jos W.R. Twisk, Fiona R.M. van der Klis, Sabine C. de Greeff, Christina M.J.E. Vandenbroucke-Grauls

Methodology and Applied Biostatistics

Research output: Contribution to Journal › Article › Academic › peer-review

Abstract

BACKGROUND: Gastric acid-suppressive therapy has been suggested to increase the risk for intestinal carriage of MDR Enterobacterales, but there is scarce community-based evidence substantiating this risk. OBJECTIVES: To investigate if acid-suppressant use is associated with a risk of intestinal carriage of ESBL and carbapenemase-producing Enterobacterales (ESBL-E) in the open population, and to assess possible modifying factors. METHODS: Within the framework of a nationwide seroprevalence study, we identified a population-based cross-sectional cohort comprising 2746 adults (≥18 years), who provided stool specimens between February 2016 and June 2017. Specimens were tested by phenotypic assays and confirmatory genotype analysis to detect carriage of ESBL-E. Covariate data were extracted from self-administered questionnaires. ORs and 95% CIs were estimated using multivariable multilevel logistic regression, controlling for confounders informed by directed acyclic graphs. RESULTS: Among 2746 participants, 316 (11.5%) used acid suppressants; the prevalence of ESBL-E carriage was 7.4% (95% CI, 6.1%-8.6%). Current use of acid suppressants was not associated with ESBL-E carriage (adjusted OR [aOR], 1.05; 95% CI, 0.64-1.74); lifestyle and comorbidity did not modify this association. A higher BMI (≥25 kg/m2) (aOR, 1.42 [95% CI, 1.02-1.98]), non-Western ethnic origin (aOR, 1.96 [95% CI, 1.34-2.87]), travel to Eastern-Mediterranean, Western-Pacific or South-East Asia regions (aOR, 3.16 [95% CI, 1.71-5.83]) were associated with ESBL-E carriage. Sensitivity analyses confirmed these results; spline analysis supported a BMI-associated risk. CONCLUSIONS: In this open population study, current use of acid suppressants was not associated with ESBL-E carriage. Travel to high-endemic regions and non-Western ethnicity were confirmed as risk factors, while a higher BMI emerged as a potential new risk for ESBL-E carriage.

Original language	English
Pages (from-to)	237-245
Number of pages	9
Journal	The Journal of antimicrobial chemotherapy
Volume	77
Issue number	1
Early online date	22 Sept 2021
DOIs	https://doi.org/10.1093/jac/dkab345
Publication status	Published - Jan 2022

Bibliographical note

Publisher Copyright:
© The Author(s) 2021. Published by Oxford University Press on behalf of the British Society for Antimicrobial Chemotherapy.

Funding

This work was supported by the Netherlands Organization for Health Research and Development (ZonMw) grant as part of the Suppression of Gastric Acid and Antimicrobial Resistance (SUGAR) project (grant number: 541001010). The funder had no role in the design and conduct of the study; data collection, analysis and interpretation of the data; preparation, review, or the decision to submit the manuscript for publication.

Funders	Funder number
Suppression of Gastric Acid and Antimicrobial Resistance	541001010
ZonMw

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Willems, R. P. J., van Dijk, K., Dierikx, C. M., Twisk, J. W. R., van der Klis, F. R. M., de Greeff, S. C., & Vandenbroucke-Grauls, C. M. J. E. (2022). Gastric acid suppression, lifestyle factors and intestinal carriage of ESBL and carbapenemase-producing Enterobacterales: a nationwide population-based study. The Journal of antimicrobial chemotherapy, 77(1), 237-245. https://doi.org/10.1093/jac/dkab345

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title = "Gastric acid suppression, lifestyle factors and intestinal carriage of ESBL and carbapenemase-producing Enterobacterales: a nationwide population-based study",

abstract = "BACKGROUND: Gastric acid-suppressive therapy has been suggested to increase the risk for intestinal carriage of MDR Enterobacterales, but there is scarce community-based evidence substantiating this risk. OBJECTIVES: To investigate if acid-suppressant use is associated with a risk of intestinal carriage of ESBL and carbapenemase-producing Enterobacterales (ESBL-E) in the open population, and to assess possible modifying factors. METHODS: Within the framework of a nationwide seroprevalence study, we identified a population-based cross-sectional cohort comprising 2746 adults (≥18 years), who provided stool specimens between February 2016 and June 2017. Specimens were tested by phenotypic assays and confirmatory genotype analysis to detect carriage of ESBL-E. Covariate data were extracted from self-administered questionnaires. ORs and 95% CIs were estimated using multivariable multilevel logistic regression, controlling for confounders informed by directed acyclic graphs. RESULTS: Among 2746 participants, 316 (11.5%) used acid suppressants; the prevalence of ESBL-E carriage was 7.4% (95% CI, 6.1%-8.6%). Current use of acid suppressants was not associated with ESBL-E carriage (adjusted OR [aOR], 1.05; 95% CI, 0.64-1.74); lifestyle and comorbidity did not modify this association. A higher BMI (≥25 kg/m2) (aOR, 1.42 [95% CI, 1.02-1.98]), non-Western ethnic origin (aOR, 1.96 [95% CI, 1.34-2.87]), travel to Eastern-Mediterranean, Western-Pacific or South-East Asia regions (aOR, 3.16 [95% CI, 1.71-5.83]) were associated with ESBL-E carriage. Sensitivity analyses confirmed these results; spline analysis supported a BMI-associated risk. CONCLUSIONS: In this open population study, current use of acid suppressants was not associated with ESBL-E carriage. Travel to high-endemic regions and non-Western ethnicity were confirmed as risk factors, while a higher BMI emerged as a potential new risk for ESBL-E carriage.",

author = "Willems, {Roel P.J.} and {van Dijk}, Karin and Dierikx, {Cindy M.} and Twisk, {Jos W.R.} and {van der Klis}, {Fiona R.M.} and {de Greeff}, {Sabine C.} and Vandenbroucke-Grauls, {Christina M.J.E.}",

note = "Publisher Copyright: {\textcopyright} The Author(s) 2021. Published by Oxford University Press on behalf of the British Society for Antimicrobial Chemotherapy.",

year = "2022",

month = jan,

doi = "10.1093/jac/dkab345",

language = "English",

volume = "77",

pages = "237--245",

journal = "The Journal of antimicrobial chemotherapy",

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Willems, RPJ, van Dijk, K, Dierikx, CM, Twisk, JWR, van der Klis, FRM, de Greeff, SC & Vandenbroucke-Grauls, CMJE 2022, 'Gastric acid suppression, lifestyle factors and intestinal carriage of ESBL and carbapenemase-producing Enterobacterales: a nationwide population-based study', The Journal of antimicrobial chemotherapy, vol. 77, no. 1, pp. 237-245. https://doi.org/10.1093/jac/dkab345

Gastric acid suppression, lifestyle factors and intestinal carriage of ESBL and carbapenemase-producing Enterobacterales: a nationwide population-based study. / Willems, Roel P.J.; van Dijk, Karin; Dierikx, Cindy M. et al.
In: The Journal of antimicrobial chemotherapy, Vol. 77, No. 1, 01.2022, p. 237-245.

Research output: Contribution to Journal › Article › Academic › peer-review

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T1 - Gastric acid suppression, lifestyle factors and intestinal carriage of ESBL and carbapenemase-producing Enterobacterales

T2 - a nationwide population-based study

AU - Willems, Roel P.J.

AU - van Dijk, Karin

AU - Dierikx, Cindy M.

AU - Twisk, Jos W.R.

AU - van der Klis, Fiona R.M.

AU - de Greeff, Sabine C.

AU - Vandenbroucke-Grauls, Christina M.J.E.

PY - 2022/1

Y1 - 2022/1

N2 - BACKGROUND: Gastric acid-suppressive therapy has been suggested to increase the risk for intestinal carriage of MDR Enterobacterales, but there is scarce community-based evidence substantiating this risk. OBJECTIVES: To investigate if acid-suppressant use is associated with a risk of intestinal carriage of ESBL and carbapenemase-producing Enterobacterales (ESBL-E) in the open population, and to assess possible modifying factors. METHODS: Within the framework of a nationwide seroprevalence study, we identified a population-based cross-sectional cohort comprising 2746 adults (≥18 years), who provided stool specimens between February 2016 and June 2017. Specimens were tested by phenotypic assays and confirmatory genotype analysis to detect carriage of ESBL-E. Covariate data were extracted from self-administered questionnaires. ORs and 95% CIs were estimated using multivariable multilevel logistic regression, controlling for confounders informed by directed acyclic graphs. RESULTS: Among 2746 participants, 316 (11.5%) used acid suppressants; the prevalence of ESBL-E carriage was 7.4% (95% CI, 6.1%-8.6%). Current use of acid suppressants was not associated with ESBL-E carriage (adjusted OR [aOR], 1.05; 95% CI, 0.64-1.74); lifestyle and comorbidity did not modify this association. A higher BMI (≥25 kg/m2) (aOR, 1.42 [95% CI, 1.02-1.98]), non-Western ethnic origin (aOR, 1.96 [95% CI, 1.34-2.87]), travel to Eastern-Mediterranean, Western-Pacific or South-East Asia regions (aOR, 3.16 [95% CI, 1.71-5.83]) were associated with ESBL-E carriage. Sensitivity analyses confirmed these results; spline analysis supported a BMI-associated risk. CONCLUSIONS: In this open population study, current use of acid suppressants was not associated with ESBL-E carriage. Travel to high-endemic regions and non-Western ethnicity were confirmed as risk factors, while a higher BMI emerged as a potential new risk for ESBL-E carriage.

AB - BACKGROUND: Gastric acid-suppressive therapy has been suggested to increase the risk for intestinal carriage of MDR Enterobacterales, but there is scarce community-based evidence substantiating this risk. OBJECTIVES: To investigate if acid-suppressant use is associated with a risk of intestinal carriage of ESBL and carbapenemase-producing Enterobacterales (ESBL-E) in the open population, and to assess possible modifying factors. METHODS: Within the framework of a nationwide seroprevalence study, we identified a population-based cross-sectional cohort comprising 2746 adults (≥18 years), who provided stool specimens between February 2016 and June 2017. Specimens were tested by phenotypic assays and confirmatory genotype analysis to detect carriage of ESBL-E. Covariate data were extracted from self-administered questionnaires. ORs and 95% CIs were estimated using multivariable multilevel logistic regression, controlling for confounders informed by directed acyclic graphs. RESULTS: Among 2746 participants, 316 (11.5%) used acid suppressants; the prevalence of ESBL-E carriage was 7.4% (95% CI, 6.1%-8.6%). Current use of acid suppressants was not associated with ESBL-E carriage (adjusted OR [aOR], 1.05; 95% CI, 0.64-1.74); lifestyle and comorbidity did not modify this association. A higher BMI (≥25 kg/m2) (aOR, 1.42 [95% CI, 1.02-1.98]), non-Western ethnic origin (aOR, 1.96 [95% CI, 1.34-2.87]), travel to Eastern-Mediterranean, Western-Pacific or South-East Asia regions (aOR, 3.16 [95% CI, 1.71-5.83]) were associated with ESBL-E carriage. Sensitivity analyses confirmed these results; spline analysis supported a BMI-associated risk. CONCLUSIONS: In this open population study, current use of acid suppressants was not associated with ESBL-E carriage. Travel to high-endemic regions and non-Western ethnicity were confirmed as risk factors, while a higher BMI emerged as a potential new risk for ESBL-E carriage.

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Gastric acid suppression, lifestyle factors and intestinal carriage of ESBL and carbapenemase-producing Enterobacterales: a nationwide population-based study

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