Impact of oral amoxicillin and amoxicillin/clavulanic acid treatment on bacterial diversity and β-lactam resistance in the canine faecal microbiota

Carmen Espinosa-Gongora; Lisbeth Rem Jessen; Ida Nordang Kieler; Peter Damborg; Charlotte Reinhard Bjørnvad; Dereje Dadi Gudeta; Teresa Pires Dos Santos; Frédérique Sablier-Gallis; Sakina Sayah-Jeanne; Tanguy Corbel; Agathe Nevière; Perrine Hugon; Nathalie Saint-Lu; Jean de Gunzburg; Luca Guardabassi

doi:10.1093/jac/dkz458

Impact of oral amoxicillin and amoxicillin/clavulanic acid treatment on bacterial diversity and β-lactam resistance in the canine faecal microbiota

Carmen Espinosa-Gongora, Lisbeth Rem Jessen, Ida Nordang Kieler, Peter Damborg, Charlotte Reinhard Bjørnvad, Dereje Dadi Gudeta, Teresa Pires Dos Santos, Frédérique Sablier-Gallis, Sakina Sayah-Jeanne, Tanguy Corbel, Agathe Nevière, Perrine Hugon, Nathalie Saint-Lu, Jean de Gunzburg, Luca Guardabassi

5 Citations (Scopus)

Abstract

BACKGROUND: Aminopenicillins with or without a β-lactamase inhibitor are widely used in both human and veterinary medicine. However, little is known about their differential impact on the gut microbiota and development of antimicrobial resistance.

OBJECTIVES: To investigate changes in the faecal microbiota of dogs treated with amoxicillin or amoxicillin/clavulanic acid.

METHODS: Faeces collected from 42 dogs (21 per treatment group) immediately before, during and 1 week after termination of oral treatment with amoxicillin or amoxicillin/clavulanic acid were analysed by culture and 16S rRNA gene sequence analysis.

RESULTS: In both groups, bacterial counts on ampicillin selective agar revealed an increase in the proportion of ampicillin-resistant Escherichia coli during treatment, and an increased occurrence and proportion of ampicillin-resistant enterococci during and after treatment. 16S rRNA gene analysis showed reductions in microbial richness and diversity during treatment followed by a return to pre-treatment conditions approximately 1 week after cessation of amoxicillin or amoxicillin/clavulanic acid treatment. While no significant differences were observed between the effects of amoxicillin and amoxicillin/clavulanic acid on microbial richness and diversity, treatment with amoxicillin/clavulanic acid reduced the abundance of taxa that are considered part of the beneficial microbiota (such as Roseburia, Dialister and Lachnospiraceae) and enriched Escherichia, although the latter result was not corroborated by phenotypic counts.

CONCLUSIONS: Our results suggest a limited effect of clavulanic acid on selection of antimicrobial resistance and microbial richness when administered orally in combination with amoxicillin. However, combination with this β-lactamase inhibitor appears to broaden the spectrum of amoxicillin, with potential negative consequences on gut health.

Original language	English
Journal	The Journal of antimicrobial chemotherapy
ISSN	0305-7453
DOIs	https://doi.org/10.1093/jac/dkz458
Publication status	Published - 1 Feb 2020

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Espinosa-Gongora, C., Jessen, L. R., Kieler, I. N., Damborg, P., Bjørnvad, C. R., Gudeta, D. D., Pires Dos Santos, T., Sablier-Gallis, F., Sayah-Jeanne, S., Corbel, T., Nevière, A., Hugon, P., Saint-Lu, N., de Gunzburg, J., & Guardabassi, L. (2020). Impact of oral amoxicillin and amoxicillin/clavulanic acid treatment on bacterial diversity and β-lactam resistance in the canine faecal microbiota. The Journal of antimicrobial chemotherapy. https://doi.org/10.1093/jac/dkz458

Impact of oral amoxicillin and amoxicillin/clavulanic acid treatment on bacterial diversity and β-lactam resistance in the canine faecal microbiota. / Espinosa-Gongora, Carmen; Jessen, Lisbeth Rem ; Kieler, Ida Nordang et al.

In: The Journal of antimicrobial chemotherapy, 01.02.2020.

Research output: Contribution to journal › Journal article › Research › peer-review

Espinosa-Gongora, C, Jessen, LR , Kieler, IN , Damborg, P , Bjørnvad, CR, Gudeta, DD, Pires Dos Santos, T, Sablier-Gallis, F, Sayah-Jeanne, S, Corbel, T, Nevière, A, Hugon, P, Saint-Lu, N, de Gunzburg, J & Guardabassi, L 2020, 'Impact of oral amoxicillin and amoxicillin/clavulanic acid treatment on bacterial diversity and β-lactam resistance in the canine faecal microbiota', The Journal of antimicrobial chemotherapy. https://doi.org/10.1093/jac/dkz458

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title = "Impact of oral amoxicillin and amoxicillin/clavulanic acid treatment on bacterial diversity and β-lactam resistance in the canine faecal microbiota",

abstract = "BACKGROUND: Aminopenicillins with or without a β-lactamase inhibitor are widely used in both human and veterinary medicine. However, little is known about their differential impact on the gut microbiota and development of antimicrobial resistance.OBJECTIVES: To investigate changes in the faecal microbiota of dogs treated with amoxicillin or amoxicillin/clavulanic acid.METHODS: Faeces collected from 42 dogs (21 per treatment group) immediately before, during and 1 week after termination of oral treatment with amoxicillin or amoxicillin/clavulanic acid were analysed by culture and 16S rRNA gene sequence analysis.RESULTS: In both groups, bacterial counts on ampicillin selective agar revealed an increase in the proportion of ampicillin-resistant Escherichia coli during treatment, and an increased occurrence and proportion of ampicillin-resistant enterococci during and after treatment. 16S rRNA gene analysis showed reductions in microbial richness and diversity during treatment followed by a return to pre-treatment conditions approximately 1 week after cessation of amoxicillin or amoxicillin/clavulanic acid treatment. While no significant differences were observed between the effects of amoxicillin and amoxicillin/clavulanic acid on microbial richness and diversity, treatment with amoxicillin/clavulanic acid reduced the abundance of taxa that are considered part of the beneficial microbiota (such as Roseburia, Dialister and Lachnospiraceae) and enriched Escherichia, although the latter result was not corroborated by phenotypic counts.CONCLUSIONS: Our results suggest a limited effect of clavulanic acid on selection of antimicrobial resistance and microbial richness when administered orally in combination with amoxicillin. However, combination with this β-lactamase inhibitor appears to broaden the spectrum of amoxicillin, with potential negative consequences on gut health.",

author = "Carmen Espinosa-Gongora and Jessen, {Lisbeth Rem} and Kieler, {Ida Nordang} and Peter Damborg and Bj{\o}rnvad, {Charlotte Reinhard} and Gudeta, {Dereje Dadi} and {Pires Dos Santos}, Teresa and Fr{\'e}d{\'e}rique Sablier-Gallis and Sakina Sayah-Jeanne and Tanguy Corbel and Agathe Nevi{\`e}re and Perrine Hugon and Nathalie Saint-Lu and {de Gunzburg}, Jean and Luca Guardabassi",

note = "{\textcopyright} The Author(s) 2019. Published by Oxford University Press on behalf of the British Society for Antimicrobial Chemotherapy. All rights reserved. For permissions, please email: [email protected].",

year = "2020",

month = feb,

day = "1",

doi = "10.1093/jac/dkz458",

language = "English",

journal = "Journal of Antimicrobial Chemotherapy",

issn = "0305-7453",

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TY - JOUR

T1 - Impact of oral amoxicillin and amoxicillin/clavulanic acid treatment on bacterial diversity and β-lactam resistance in the canine faecal microbiota

AU - Espinosa-Gongora, Carmen

AU - Jessen, Lisbeth Rem

AU - Kieler, Ida Nordang

AU - Damborg, Peter

AU - Bjørnvad, Charlotte Reinhard

AU - Gudeta, Dereje Dadi

AU - Pires Dos Santos, Teresa

AU - Sablier-Gallis, Frédérique

AU - Sayah-Jeanne, Sakina

AU - Corbel, Tanguy

AU - Nevière, Agathe

AU - Hugon, Perrine

AU - Saint-Lu, Nathalie

AU - de Gunzburg, Jean

AU - Guardabassi, Luca

PY - 2020/2/1

Y1 - 2020/2/1

N2 - BACKGROUND: Aminopenicillins with or without a β-lactamase inhibitor are widely used in both human and veterinary medicine. However, little is known about their differential impact on the gut microbiota and development of antimicrobial resistance.OBJECTIVES: To investigate changes in the faecal microbiota of dogs treated with amoxicillin or amoxicillin/clavulanic acid.METHODS: Faeces collected from 42 dogs (21 per treatment group) immediately before, during and 1 week after termination of oral treatment with amoxicillin or amoxicillin/clavulanic acid were analysed by culture and 16S rRNA gene sequence analysis.RESULTS: In both groups, bacterial counts on ampicillin selective agar revealed an increase in the proportion of ampicillin-resistant Escherichia coli during treatment, and an increased occurrence and proportion of ampicillin-resistant enterococci during and after treatment. 16S rRNA gene analysis showed reductions in microbial richness and diversity during treatment followed by a return to pre-treatment conditions approximately 1 week after cessation of amoxicillin or amoxicillin/clavulanic acid treatment. While no significant differences were observed between the effects of amoxicillin and amoxicillin/clavulanic acid on microbial richness and diversity, treatment with amoxicillin/clavulanic acid reduced the abundance of taxa that are considered part of the beneficial microbiota (such as Roseburia, Dialister and Lachnospiraceae) and enriched Escherichia, although the latter result was not corroborated by phenotypic counts.CONCLUSIONS: Our results suggest a limited effect of clavulanic acid on selection of antimicrobial resistance and microbial richness when administered orally in combination with amoxicillin. However, combination with this β-lactamase inhibitor appears to broaden the spectrum of amoxicillin, with potential negative consequences on gut health.

AB - BACKGROUND: Aminopenicillins with or without a β-lactamase inhibitor are widely used in both human and veterinary medicine. However, little is known about their differential impact on the gut microbiota and development of antimicrobial resistance.OBJECTIVES: To investigate changes in the faecal microbiota of dogs treated with amoxicillin or amoxicillin/clavulanic acid.METHODS: Faeces collected from 42 dogs (21 per treatment group) immediately before, during and 1 week after termination of oral treatment with amoxicillin or amoxicillin/clavulanic acid were analysed by culture and 16S rRNA gene sequence analysis.RESULTS: In both groups, bacterial counts on ampicillin selective agar revealed an increase in the proportion of ampicillin-resistant Escherichia coli during treatment, and an increased occurrence and proportion of ampicillin-resistant enterococci during and after treatment. 16S rRNA gene analysis showed reductions in microbial richness and diversity during treatment followed by a return to pre-treatment conditions approximately 1 week after cessation of amoxicillin or amoxicillin/clavulanic acid treatment. While no significant differences were observed between the effects of amoxicillin and amoxicillin/clavulanic acid on microbial richness and diversity, treatment with amoxicillin/clavulanic acid reduced the abundance of taxa that are considered part of the beneficial microbiota (such as Roseburia, Dialister and Lachnospiraceae) and enriched Escherichia, although the latter result was not corroborated by phenotypic counts.CONCLUSIONS: Our results suggest a limited effect of clavulanic acid on selection of antimicrobial resistance and microbial richness when administered orally in combination with amoxicillin. However, combination with this β-lactamase inhibitor appears to broaden the spectrum of amoxicillin, with potential negative consequences on gut health.

U2 - 10.1093/jac/dkz458

DO - 10.1093/jac/dkz458

M3 - Journal article

C2 - 31778166

SN - 0305-7453

JO - Journal of Antimicrobial Chemotherapy

JF - Journal of Antimicrobial Chemotherapy

ER -

Impact of oral amoxicillin and amoxicillin/clavulanic acid treatment on bacterial diversity and β-lactam resistance in the canine faecal microbiota

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