Temporal association of antimicrobial use in livestock with antimicrobial resistance in non-typhoid Salmonella human infections in the Netherlands, 2008–2019

Linda E. Chanamé Pinedo; Anouk P. Meijs; Huifang Deng; Sabine C. de Greeff; Engeline van Duijkeren; Cindy M. Dierikx; Kees T. Veldman; Pim Sanders; Maaike J.C. van den Beld; Bart Wullings; Eelco Franz; Roan Pijnacker; Lapo Mughini-Gras

doi:10.1016/j.onehlt.2024.100844

Temporal association of antimicrobial use in livestock with antimicrobial resistance in non-typhoid Salmonella human infections in the Netherlands, 2008–2019

Linda E. Chanamé Pinedo^*, Anouk P. Meijs, Huifang Deng, Sabine C. de Greeff, Engeline van Duijkeren, Cindy M. Dierikx, Kees T. Veldman, Pim Sanders, Maaike J.C. van den Beld, Bart Wullings, Eelco Franz, Roan Pijnacker, Lapo Mughini-Gras

^*Corresponding author for this work

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

Abstract

Background: Antimicrobial use (AMU) in livestock contributes to antimicrobial resistance (AMR) among zoonotic pathogens, such as non-typhoid Salmonella (NTS). Since 2009, the Netherlands has made substantial efforts to reduce AMU in livestock. Objectives: To assess the association between AMU in livestock and AMR in NTS human isolates. Additionally, associations between AMU in broilers/pigs and AMR in NTS broiler/pig isolates, and between AMR in broilers/pigs and in human NTS isolates were assessed. The focus was on Salmonella Enteritidis (SE) and Salmonella Typhimurium including its monophasic variant (ST/STM). Methods: A national population registry-based study was conducted in the Netherlands from 2008 to 2019. Multivariable logistic regression models were used to assess the associations between livestock AMU and NTS resistance proportion in humans and broilers/pigs, overall as well as per class-specific antimicrobials. Correlation analysis was performed to relate AMR proportions between human and broiler/pig NTS isolates. Results: For SE, only a positive association between penicillins use in broilers and resistance to ampicillin among human isolates was significant. For ST/STM, most associations between AMU in livestock and AMR among human isolates were significantly positive, overall and per class-specific antimicrobials, namely for penicillins-ampicillin, tetracyclines-tetracycline and sulfonamides/trimethoprim-sulfamethoxazole/trimethoprim. Significantly positive associations between AMU in broilers/pigs and AMR in broiler/pig ST/STM isolates were also observed, but not between broiler/pig and human AMR levels. Conclusions: Significant associations were generally found between livestock AMU and AMR in human and broiler/pig ST/STM isolates. However, confounding factors, such as imported meat and travel are of concern. To fully comprehend the impact of livestock AMU on resistance in human NTS isolates, it is imperative to enhance AMR surveillance of NTS.

Original language	English
Article number	100844
Journal	One Health
Volume	19
DOIs	https://doi.org/10.1016/j.onehlt.2024.100844
Publication status	Published - Dec 2024

Bibliographical note

Publisher Copyright:
© 2024 The Authors

Funding

This study was supported by the research project "Effects decreaSing AntiBiotic use in animaLs on antibiotic reSistance in infections" (EStABLiSH) funded through the Netherlands Organization for Health Research and Development (ZonMw) (Grant 541003002) .

Funders	Funder number
Netherlands Organization for Health Research and Development (ZonMw)	541003002

Keywords

Antimicrobial use
Drug resistance
Livestock
Salmonellosis

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1016/j.onehlt.2024.100844Licence: CC BY-NC

1-s2.0-S2352771424001708-mainFinal published version, 1.32 MBLicence: CC BY-NC

Cite this

Chanamé Pinedo, L. E., Meijs, A. P., Deng, H., de Greeff, S. C., van Duijkeren, E., Dierikx, C. M., Veldman, K. T., Sanders, P., van den Beld, M. J. C., Wullings, B., Franz, E., Pijnacker, R., & Mughini-Gras, L. (2024). Temporal association of antimicrobial use in livestock with antimicrobial resistance in non-typhoid Salmonella human infections in the Netherlands, 2008–2019. One Health, 19, Article 100844. https://doi.org/10.1016/j.onehlt.2024.100844

@article{03e611667d3141cda037393f801d413d,

title = "Temporal association of antimicrobial use in livestock with antimicrobial resistance in non-typhoid Salmonella human infections in the Netherlands, 2008–2019",

abstract = "Background: Antimicrobial use (AMU) in livestock contributes to antimicrobial resistance (AMR) among zoonotic pathogens, such as non-typhoid Salmonella (NTS). Since 2009, the Netherlands has made substantial efforts to reduce AMU in livestock. Objectives: To assess the association between AMU in livestock and AMR in NTS human isolates. Additionally, associations between AMU in broilers/pigs and AMR in NTS broiler/pig isolates, and between AMR in broilers/pigs and in human NTS isolates were assessed. The focus was on Salmonella Enteritidis (SE) and Salmonella Typhimurium including its monophasic variant (ST/STM). Methods: A national population registry-based study was conducted in the Netherlands from 2008 to 2019. Multivariable logistic regression models were used to assess the associations between livestock AMU and NTS resistance proportion in humans and broilers/pigs, overall as well as per class-specific antimicrobials. Correlation analysis was performed to relate AMR proportions between human and broiler/pig NTS isolates. Results: For SE, only a positive association between penicillins use in broilers and resistance to ampicillin among human isolates was significant. For ST/STM, most associations between AMU in livestock and AMR among human isolates were significantly positive, overall and per class-specific antimicrobials, namely for penicillins-ampicillin, tetracyclines-tetracycline and sulfonamides/trimethoprim-sulfamethoxazole/trimethoprim. Significantly positive associations between AMU in broilers/pigs and AMR in broiler/pig ST/STM isolates were also observed, but not between broiler/pig and human AMR levels. Conclusions: Significant associations were generally found between livestock AMU and AMR in human and broiler/pig ST/STM isolates. However, confounding factors, such as imported meat and travel are of concern. To fully comprehend the impact of livestock AMU on resistance in human NTS isolates, it is imperative to enhance AMR surveillance of NTS.",

keywords = "Antimicrobial use, Drug resistance, Livestock, Salmonellosis",

author = "{Chanam{\'e} Pinedo}, {Linda E.} and Meijs, {Anouk P.} and Huifang Deng and {de Greeff}, {Sabine C.} and {van Duijkeren}, Engeline and Dierikx, {Cindy M.} and Veldman, {Kees T.} and Pim Sanders and {van den Beld}, {Maaike J.C.} and Bart Wullings and Eelco Franz and Roan Pijnacker and Lapo Mughini-Gras",

note = "Publisher Copyright: {\textcopyright} 2024 The Authors",

year = "2024",

month = dec,

doi = "10.1016/j.onehlt.2024.100844",

language = "English",

volume = "19",

journal = "One Health",

issn = "1949-4998",

publisher = "Elsevier BV",

}

Chanamé Pinedo, LE, Meijs, AP, Deng, H, de Greeff, SC, van Duijkeren, E, Dierikx, CM, Veldman, KT, Sanders, P, van den Beld, MJC, Wullings, B, Franz, E, Pijnacker, R & Mughini-Gras, L 2024, 'Temporal association of antimicrobial use in livestock with antimicrobial resistance in non-typhoid Salmonella human infections in the Netherlands, 2008–2019', One Health, vol. 19, 100844. https://doi.org/10.1016/j.onehlt.2024.100844

TY - JOUR

T1 - Temporal association of antimicrobial use in livestock with antimicrobial resistance in non-typhoid Salmonella human infections in the Netherlands, 2008–2019

AU - Chanamé Pinedo, Linda E.

AU - Meijs, Anouk P.

AU - Deng, Huifang

AU - de Greeff, Sabine C.

AU - van Duijkeren, Engeline

AU - Dierikx, Cindy M.

AU - Veldman, Kees T.

AU - Sanders, Pim

AU - van den Beld, Maaike J.C.

AU - Wullings, Bart

AU - Franz, Eelco

AU - Pijnacker, Roan

AU - Mughini-Gras, Lapo

PY - 2024/12

Y1 - 2024/12

N2 - Background: Antimicrobial use (AMU) in livestock contributes to antimicrobial resistance (AMR) among zoonotic pathogens, such as non-typhoid Salmonella (NTS). Since 2009, the Netherlands has made substantial efforts to reduce AMU in livestock. Objectives: To assess the association between AMU in livestock and AMR in NTS human isolates. Additionally, associations between AMU in broilers/pigs and AMR in NTS broiler/pig isolates, and between AMR in broilers/pigs and in human NTS isolates were assessed. The focus was on Salmonella Enteritidis (SE) and Salmonella Typhimurium including its monophasic variant (ST/STM). Methods: A national population registry-based study was conducted in the Netherlands from 2008 to 2019. Multivariable logistic regression models were used to assess the associations between livestock AMU and NTS resistance proportion in humans and broilers/pigs, overall as well as per class-specific antimicrobials. Correlation analysis was performed to relate AMR proportions between human and broiler/pig NTS isolates. Results: For SE, only a positive association between penicillins use in broilers and resistance to ampicillin among human isolates was significant. For ST/STM, most associations between AMU in livestock and AMR among human isolates were significantly positive, overall and per class-specific antimicrobials, namely for penicillins-ampicillin, tetracyclines-tetracycline and sulfonamides/trimethoprim-sulfamethoxazole/trimethoprim. Significantly positive associations between AMU in broilers/pigs and AMR in broiler/pig ST/STM isolates were also observed, but not between broiler/pig and human AMR levels. Conclusions: Significant associations were generally found between livestock AMU and AMR in human and broiler/pig ST/STM isolates. However, confounding factors, such as imported meat and travel are of concern. To fully comprehend the impact of livestock AMU on resistance in human NTS isolates, it is imperative to enhance AMR surveillance of NTS.

AB - Background: Antimicrobial use (AMU) in livestock contributes to antimicrobial resistance (AMR) among zoonotic pathogens, such as non-typhoid Salmonella (NTS). Since 2009, the Netherlands has made substantial efforts to reduce AMU in livestock. Objectives: To assess the association between AMU in livestock and AMR in NTS human isolates. Additionally, associations between AMU in broilers/pigs and AMR in NTS broiler/pig isolates, and between AMR in broilers/pigs and in human NTS isolates were assessed. The focus was on Salmonella Enteritidis (SE) and Salmonella Typhimurium including its monophasic variant (ST/STM). Methods: A national population registry-based study was conducted in the Netherlands from 2008 to 2019. Multivariable logistic regression models were used to assess the associations between livestock AMU and NTS resistance proportion in humans and broilers/pigs, overall as well as per class-specific antimicrobials. Correlation analysis was performed to relate AMR proportions between human and broiler/pig NTS isolates. Results: For SE, only a positive association between penicillins use in broilers and resistance to ampicillin among human isolates was significant. For ST/STM, most associations between AMU in livestock and AMR among human isolates were significantly positive, overall and per class-specific antimicrobials, namely for penicillins-ampicillin, tetracyclines-tetracycline and sulfonamides/trimethoprim-sulfamethoxazole/trimethoprim. Significantly positive associations between AMU in broilers/pigs and AMR in broiler/pig ST/STM isolates were also observed, but not between broiler/pig and human AMR levels. Conclusions: Significant associations were generally found between livestock AMU and AMR in human and broiler/pig ST/STM isolates. However, confounding factors, such as imported meat and travel are of concern. To fully comprehend the impact of livestock AMU on resistance in human NTS isolates, it is imperative to enhance AMR surveillance of NTS.

KW - Antimicrobial use

KW - Drug resistance

KW - Livestock

KW - Salmonellosis

UR - http://www.scopus.com/inward/record.url?scp=85196631351&partnerID=8YFLogxK

U2 - 10.1016/j.onehlt.2024.100844

DO - 10.1016/j.onehlt.2024.100844

M3 - Article

AN - SCOPUS:85196631351

SN - 1949-4998

VL - 19

JO - One Health

JF - One Health

M1 - 100844

ER -

Temporal association of antimicrobial use in livestock with antimicrobial resistance in non-typhoid Salmonella human infections in the Netherlands, 2008–2019

Abstract

Bibliographical note

Funding

Keywords

UN SDGs

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