Effects of selective digestive decontamination (SDD) on the gut resistome

Elena Buelow; Teresita Bello Gonzalez; Dennis Versluis; Evelien A N Oostdijk; Lesley A Ogilvie; Maaike S M van Mourik; Els Oosterink; Mark W J van Passel; Hauke Smidt; Marco Maria D'Andrea; Mark de Been; Brian V Jones; Rob J L Willems; Marc J M Bonten; Willem van Schaik

doi:10.1093/jac/dku092

Effects of selective digestive decontamination (SDD) on the gut resistome

Elena Buelow, Teresita Bello Gonzalez, Dennis Versluis, Evelien A N Oostdijk, Lesley A Ogilvie, Maaike S M van Mourik, Els Oosterink, Mark W J van Passel, Hauke Smidt, Marco Maria D'Andrea, Mark de Been, Brian V Jones, Rob J L Willems, Marc J M Bonten, Willem van Schaik

Department of Life Sciences

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

82 Citations (SciVal)

Abstract

OBJECTIVES: Selective digestive decontamination (SDD) is an infection prevention measure for critically ill patients in intensive care units (ICUs) that aims to eradicate opportunistic pathogens from the oropharynx and intestines, while sparing the anaerobic flora, by the application of non-absorbable antibiotics. Selection for antibiotic-resistant bacteria is still a major concern for SDD. We therefore studied the impact of SDD on the reservoir of antibiotic resistance genes (i.e. the resistome) by culture-independent approaches.

METHODS: We evaluated the impact of SDD on the gut microbiota and resistome in a single ICU patient during and after an ICU stay by several metagenomic approaches. We also determined by quantitative PCR the relative abundance of two common aminoglycoside resistance genes in longitudinally collected samples from 12 additional ICU patients who received SDD.

RESULTS: The patient microbiota was highly dynamic during the hospital stay. The abundance of antibiotic resistance genes more than doubled during SDD use, mainly due to a 6.7-fold increase in aminoglycoside resistance genes, in particular aph(2″)-Ib and an aadE-like gene. We show that aph(2″)-Ib is harboured by anaerobic gut commensals and is associated with mobile genetic elements. In longitudinal samples of 12 ICU patients, the dynamics of these two genes ranged from a ∼10(4) fold increase to a ∼10(-10) fold decrease in relative abundance during SDD.

CONCLUSIONS: ICU hospitalization and the simultaneous application of SDD has large, but highly individualized, effects on the gut resistome of ICU patients. Selection for transferable antibiotic resistance genes in anaerobic commensal bacteria could impact the risk of transfer of antibiotic resistance genes to opportunistic pathogens.

Original language	English
Pages (from-to)	2215-23
Number of pages	9
Journal	Journal of Antimicrobial Chemotherapy
Volume	69
Issue number	8
Early online date	7 Apr 2014
DOIs	https://doi.org/10.1093/jac/dku092
Publication status	Published - 1 Aug 2014

Keywords

Anti-Bacterial Agents/administration & dosage
Bacterial Typing Techniques
Base Sequence
Clostridium/drug effects
Critical Care
DNA, Bacterial/genetics
Decontamination/methods
Drug Resistance, Bacterial/genetics
Feces/microbiology
Humans
Intestines/microbiology
Male
Microbiota/drug effects
Molecular Sequence Data
Oropharynx/microbiology
Phosphotransferases (Alcohol Group Acceptor)/genetics
RNA, Ribosomal, 16S/genetics
Sequence Analysis, DNA
Symbiosis

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10.1093/jac/dku092

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Buelow, E., Gonzalez, T. B., Versluis, D., Oostdijk, E. A. N., Ogilvie, L. A., van Mourik, M. S. M., Oosterink, E., van Passel, M. W. J., Smidt, H., D'Andrea, M. M., de Been, M., Jones, B. V., Willems, R. J. L., Bonten, M. J. M., & van Schaik, W. (2014). Effects of selective digestive decontamination (SDD) on the gut resistome. Journal of Antimicrobial Chemotherapy, 69(8), 2215-23. https://doi.org/10.1093/jac/dku092

Buelow, E, Gonzalez, TB, Versluis, D, Oostdijk, EAN, Ogilvie, LA, van Mourik, MSM, Oosterink, E, van Passel, MWJ, Smidt, H, D'Andrea, MM, de Been, M, Jones, BV, Willems, RJL, Bonten, MJM & van Schaik, W 2014, 'Effects of selective digestive decontamination (SDD) on the gut resistome', Journal of Antimicrobial Chemotherapy, vol. 69, no. 8, pp. 2215-23. https://doi.org/10.1093/jac/dku092

@article{7fb921ba5da34d0f83c41bd4679527bc,

title = "Effects of selective digestive decontamination (SDD) on the gut resistome",

abstract = "OBJECTIVES: Selective digestive decontamination (SDD) is an infection prevention measure for critically ill patients in intensive care units (ICUs) that aims to eradicate opportunistic pathogens from the oropharynx and intestines, while sparing the anaerobic flora, by the application of non-absorbable antibiotics. Selection for antibiotic-resistant bacteria is still a major concern for SDD. We therefore studied the impact of SDD on the reservoir of antibiotic resistance genes (i.e. the resistome) by culture-independent approaches.METHODS: We evaluated the impact of SDD on the gut microbiota and resistome in a single ICU patient during and after an ICU stay by several metagenomic approaches. We also determined by quantitative PCR the relative abundance of two common aminoglycoside resistance genes in longitudinally collected samples from 12 additional ICU patients who received SDD.RESULTS: The patient microbiota was highly dynamic during the hospital stay. The abundance of antibiotic resistance genes more than doubled during SDD use, mainly due to a 6.7-fold increase in aminoglycoside resistance genes, in particular aph(2″)-Ib and an aadE-like gene. We show that aph(2″)-Ib is harboured by anaerobic gut commensals and is associated with mobile genetic elements. In longitudinal samples of 12 ICU patients, the dynamics of these two genes ranged from a ∼10(4) fold increase to a ∼10(-10) fold decrease in relative abundance during SDD.CONCLUSIONS: ICU hospitalization and the simultaneous application of SDD has large, but highly individualized, effects on the gut resistome of ICU patients. Selection for transferable antibiotic resistance genes in anaerobic commensal bacteria could impact the risk of transfer of antibiotic resistance genes to opportunistic pathogens.",

keywords = "Anti-Bacterial Agents/administration & dosage, Bacterial Typing Techniques, Base Sequence, Clostridium/drug effects, Critical Care, DNA, Bacterial/genetics, Decontamination/methods, Drug Resistance, Bacterial/genetics, Feces/microbiology, Humans, Intestines/microbiology, Male, Microbiota/drug effects, Molecular Sequence Data, Oropharynx/microbiology, Phosphotransferases (Alcohol Group Acceptor)/genetics, RNA, Ribosomal, 16S/genetics, Sequence Analysis, DNA, Symbiosis",

author = "Elena Buelow and Gonzalez, {Teresita Bello} and Dennis Versluis and Oostdijk, {Evelien A N} and Ogilvie, {Lesley A} and {van Mourik}, {Maaike S M} and Els Oosterink and {van Passel}, {Mark W J} and Hauke Smidt and D'Andrea, {Marco Maria} and {de Been}, Mark and Jones, {Brian V} and Willems, {Rob J L} and Bonten, {Marc J M} and {van Schaik}, Willem",

note = "{\textcopyright} The Author 2014. Published by Oxford University Press on behalf of the British Society for Antimicrobial Chemotherapy. All rights reserved. For Permissions, please e-mail: [email protected].",

year = "2014",

month = aug,

day = "1",

doi = "10.1093/jac/dku092",

language = "English",

volume = "69",

pages = "2215--23",

journal = "Journal of Antimicrobial Chemotherapy",

issn = "0305-7453",

publisher = "Oxford University Press",

number = "8",

}

TY - JOUR

T1 - Effects of selective digestive decontamination (SDD) on the gut resistome

AU - Buelow, Elena

AU - Gonzalez, Teresita Bello

AU - Versluis, Dennis

AU - Oostdijk, Evelien A N

AU - Ogilvie, Lesley A

AU - van Mourik, Maaike S M

AU - Oosterink, Els

AU - van Passel, Mark W J

AU - Smidt, Hauke

AU - D'Andrea, Marco Maria

AU - de Been, Mark

AU - Jones, Brian V

AU - Willems, Rob J L

AU - Bonten, Marc J M

AU - van Schaik, Willem

PY - 2014/8/1

Y1 - 2014/8/1

N2 - OBJECTIVES: Selective digestive decontamination (SDD) is an infection prevention measure for critically ill patients in intensive care units (ICUs) that aims to eradicate opportunistic pathogens from the oropharynx and intestines, while sparing the anaerobic flora, by the application of non-absorbable antibiotics. Selection for antibiotic-resistant bacteria is still a major concern for SDD. We therefore studied the impact of SDD on the reservoir of antibiotic resistance genes (i.e. the resistome) by culture-independent approaches.METHODS: We evaluated the impact of SDD on the gut microbiota and resistome in a single ICU patient during and after an ICU stay by several metagenomic approaches. We also determined by quantitative PCR the relative abundance of two common aminoglycoside resistance genes in longitudinally collected samples from 12 additional ICU patients who received SDD.RESULTS: The patient microbiota was highly dynamic during the hospital stay. The abundance of antibiotic resistance genes more than doubled during SDD use, mainly due to a 6.7-fold increase in aminoglycoside resistance genes, in particular aph(2″)-Ib and an aadE-like gene. We show that aph(2″)-Ib is harboured by anaerobic gut commensals and is associated with mobile genetic elements. In longitudinal samples of 12 ICU patients, the dynamics of these two genes ranged from a ∼10(4) fold increase to a ∼10(-10) fold decrease in relative abundance during SDD.CONCLUSIONS: ICU hospitalization and the simultaneous application of SDD has large, but highly individualized, effects on the gut resistome of ICU patients. Selection for transferable antibiotic resistance genes in anaerobic commensal bacteria could impact the risk of transfer of antibiotic resistance genes to opportunistic pathogens.

AB - OBJECTIVES: Selective digestive decontamination (SDD) is an infection prevention measure for critically ill patients in intensive care units (ICUs) that aims to eradicate opportunistic pathogens from the oropharynx and intestines, while sparing the anaerobic flora, by the application of non-absorbable antibiotics. Selection for antibiotic-resistant bacteria is still a major concern for SDD. We therefore studied the impact of SDD on the reservoir of antibiotic resistance genes (i.e. the resistome) by culture-independent approaches.METHODS: We evaluated the impact of SDD on the gut microbiota and resistome in a single ICU patient during and after an ICU stay by several metagenomic approaches. We also determined by quantitative PCR the relative abundance of two common aminoglycoside resistance genes in longitudinally collected samples from 12 additional ICU patients who received SDD.RESULTS: The patient microbiota was highly dynamic during the hospital stay. The abundance of antibiotic resistance genes more than doubled during SDD use, mainly due to a 6.7-fold increase in aminoglycoside resistance genes, in particular aph(2″)-Ib and an aadE-like gene. We show that aph(2″)-Ib is harboured by anaerobic gut commensals and is associated with mobile genetic elements. In longitudinal samples of 12 ICU patients, the dynamics of these two genes ranged from a ∼10(4) fold increase to a ∼10(-10) fold decrease in relative abundance during SDD.CONCLUSIONS: ICU hospitalization and the simultaneous application of SDD has large, but highly individualized, effects on the gut resistome of ICU patients. Selection for transferable antibiotic resistance genes in anaerobic commensal bacteria could impact the risk of transfer of antibiotic resistance genes to opportunistic pathogens.

KW - Anti-Bacterial Agents/administration & dosage

KW - Bacterial Typing Techniques

KW - Base Sequence

KW - Clostridium/drug effects

KW - Critical Care

KW - DNA, Bacterial/genetics

KW - Decontamination/methods

KW - Drug Resistance, Bacterial/genetics

KW - Feces/microbiology

KW - Humans

KW - Intestines/microbiology

KW - Male

KW - Microbiota/drug effects

KW - Molecular Sequence Data

KW - Oropharynx/microbiology

KW - Phosphotransferases (Alcohol Group Acceptor)/genetics

KW - RNA, Ribosomal, 16S/genetics

KW - Sequence Analysis, DNA

KW - Symbiosis

U2 - 10.1093/jac/dku092

DO - 10.1093/jac/dku092

M3 - Article

C2 - 24710024

SN - 0305-7453

VL - 69

SP - 2215

EP - 2223

JO - Journal of Antimicrobial Chemotherapy

JF - Journal of Antimicrobial Chemotherapy

IS - 8

ER -

Effects of selective digestive decontamination (SDD) on the gut resistome

Abstract

Keywords

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