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Non-serotype 2 isolates from healthy pigs are a potential zoonotic reservoir of Streptococcus suis genetic diversity and antimicrobial resistance

Nattinee Kittiwan, View ORCID ProfileJessica K. Calland, View ORCID ProfileEvangelos Mourkas, View ORCID ProfileMatthew D. Hitchings, View ORCID ProfileSusan Murray, View ORCID ProfilePakpoom Tadee, View ORCID ProfilePacharaporn Tadee, View ORCID ProfileKwanjit Duangsonk, View ORCID ProfileGuillaume Méric, View ORCID ProfileSamuel K. Sheppard, View ORCID ProfilePrapas Patchanee, View ORCID ProfileBen Pascoe
doi: https://doi.org/10.1101/2021.06.17.447897
Nattinee Kittiwan
1Department of Food Animal Clinics, Faculty of Veterinary Medicine, Chiang Mai University, Chiang Mai, 50100, Thailand
2Integrative Research Centre for Veterinary Preventive Medicine, Faculty of Veterinary Medicine, Chiang Mai University, Chiang Mai, 50100, Thailand
3Veterinary Research and development center (Upper Northern region), Hang Chat, Lampang, 52190, Thailand
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Jessica K. Calland
4The Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, UK
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Evangelos Mourkas
4The Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, UK
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Matthew D. Hitchings
5Swansea University Medical School, Swansea University, Singleton Park, Swansea, UK
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Susan Murray
5Swansea University Medical School, Swansea University, Singleton Park, Swansea, UK
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Pakpoom Tadee
1Department of Food Animal Clinics, Faculty of Veterinary Medicine, Chiang Mai University, Chiang Mai, 50100, Thailand
2Integrative Research Centre for Veterinary Preventive Medicine, Faculty of Veterinary Medicine, Chiang Mai University, Chiang Mai, 50100, Thailand
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Pacharaporn Tadee
6Faculty of Animal Science and Technology, Maejo University, Chiang Mai, 50290, Thailand
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Kwanjit Duangsonk
7Department of Microbiology, Faculty of Medicine, Chiang Mai University, Chiang Mai, 50200, Thailand
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Guillaume Méric
4The Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, UK
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Samuel K. Sheppard
4The Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, UK
8Faculty of Allied Medical Science, Chiang Mai University, Chiang Mai, 50200, Thailand
9Department of Zoology, University of Oxford, South Parks Road, Oxford, OX1 3PS, UK
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Prapas Patchanee
1Department of Food Animal Clinics, Faculty of Veterinary Medicine, Chiang Mai University, Chiang Mai, 50100, Thailand
2Integrative Research Centre for Veterinary Preventive Medicine, Faculty of Veterinary Medicine, Chiang Mai University, Chiang Mai, 50100, Thailand
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  • For correspondence: prapas.pat@cmu.ac.th B.Pascoe@bath.ac.uk
Ben Pascoe
2Integrative Research Centre for Veterinary Preventive Medicine, Faculty of Veterinary Medicine, Chiang Mai University, Chiang Mai, 50100, Thailand
4The Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, UK
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  • For correspondence: prapas.pat@cmu.ac.th B.Pascoe@bath.ac.uk
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Summary

Streptococcus suis is a leading cause of bacterial meningitis in SE Asia, with frequent zoonotic transfer to humans associated with close contact with pigs. A small number of invasive lineages are responsible for endemic infection in the swine industry causing considerable global economic losses. A lack of surveillance and a rising trend in clinical treatment failure has raised concerns of growing antimicrobial resistance (AMR) among invasive S. suis. The source-sink dynamics between healthy and disease isolates is poorly understood and, in this study, we sample and sequence a collection of isolates predominantly from healthy pigs in Chiang Mai province, Northern Thailand. Pangenome comparisons with a selection of invasive serotype 2 isolates identified increased genetic diversity and more frequent AMR carriage in isolates from healthy pigs. Multiple antimicrobial resistance genes were identified conferring resistance to aminoglycosides, lincosamides, tetracycline and macrolides. All isolates were non-susceptinle to three or more different antimicrobial classes, and 75% of non-serotype 2 isolates were non-susceptible to 6 or more classes (compared to 37.5% of serotype 2 isolates). Antimicrobial resistance genes were found on integrative and conjugative elements (ICE) previously observed in other species, suggesting mobile gene pool which can be accessed by invasive disease isolates.

Significance statement The zoonotic pathogen Streptococcus suis causes respiratory disease in pigs and is among the most common causative agents of human clinical bacterial meningitis in SE Asia. We collected isolates from farmed healthy pigs in Northern Thailand, representing a source population from which invasive isolates have recently emerged – linked to the pork production industry. Pangenome characterisation of the isolates revealed a reservoir of genetic diversity and antimicrobial resistance suggesting that One Health approaches may be beneficial in tackling the increase in antimicrobial resistance.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://www.ncbi.nlm.nih.gov/bioproject/PRJNA418954

  • https://doi.org/10.6084/m9.figshare.13385465

  • List of abbreviations

    AMC
    Amoxycillin-Clavulanic acid
    AMP
    Ampicillin
    AMR
    Antimicrobial Resistance
    AMX
    Amoxycillin
    ARGs
    Antimicrobial Resistance Genes
    CARD
    Comprehensive Antibiotic Resistance Database
    CHL
    Chloramphenical
    CLI
    Clindamycin
    CTF
    Ceftiofur
    DOX
    Doxycycline
    ENR
    Enrofloxacin
    ERY
    Erythromycin
    FLO
    Florfenicol
    GEN
    Gentamycin
    ICE
    Integrative and Conjugative Elements
    KAN
    Kanamycin
    LIN
    Lincomycin
    LZD
    Linezolid
    MDR
    Multiple Drug Resistance
    MLS
    Macrolide-Lincosamide-Streptogramin B
    NCBI
    National Center for Biotechnology Information
    OTC
    Oxytetracyclin
    PEN
    Penicillin G
    SXT
    Sulfamethoxazole/Trimethoprim
    TET
    Tetracycline
    VFDB
    Virulence Factor Database
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    Non-serotype 2 isolates from healthy pigs are a potential zoonotic reservoir of Streptococcus suis genetic diversity and antimicrobial resistance
    Nattinee Kittiwan, Jessica K. Calland, Evangelos Mourkas, Matthew D. Hitchings, Susan Murray, Pakpoom Tadee, Pacharaporn Tadee, Kwanjit Duangsonk, Guillaume Méric, Samuel K. Sheppard, Prapas Patchanee, Ben Pascoe
    bioRxiv 2021.06.17.447897; doi: https://doi.org/10.1101/2021.06.17.447897
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    Non-serotype 2 isolates from healthy pigs are a potential zoonotic reservoir of Streptococcus suis genetic diversity and antimicrobial resistance
    Nattinee Kittiwan, Jessica K. Calland, Evangelos Mourkas, Matthew D. Hitchings, Susan Murray, Pakpoom Tadee, Pacharaporn Tadee, Kwanjit Duangsonk, Guillaume Méric, Samuel K. Sheppard, Prapas Patchanee, Ben Pascoe
    bioRxiv 2021.06.17.447897; doi: https://doi.org/10.1101/2021.06.17.447897

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