Antimicrobial Susceptibility and Resistance Genes in Streptococcus uberis Isolated from Bovine Mastitis in the Czech Republic

. 2023 Oct 11 ; 12 (10) : . [epub] 20231011

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid37887228

Grantová podpora
MZE-RO0523 Ministry of agriculture of the Czech Republic
QK1910212 Ministry of agriculture of the Czech Republic

Streptococcus uberis is one of the most important causative agents of mastitis and is a common reason for the use of antimicrobials in dairy cows. In this study, we assessed the antimicrobial susceptibility of 667 S. uberis isolates originating from 216 Czech dairy farms collected between 2019 and 2023 using the broth microdilution method. We tested 140 of the isolates for the presence of antimicrobial genes using whole-genome sequencing and evaluated their relationship with phenotypic resistance. Streptococcus uberis isolates showed high levels of resistance to tetracycline (59%), followed by streptomycin (38%) and clindamycin (29%). Although all of the isolates were susceptible to beta-lactams, a relatively high percentage of intermediately susceptible isolates was recorded for ampicillin (44%) and penicillin (18%). The isolates were mainly resistant to tetracycline alone (31.3%); the second most frequent occurrence of the phenotypic profile was simultaneous resistance to tetracycline, streptomycin, and clindamycin (16.6%). The occurrence of antibiotic resistance genes did not always match the phenotypic results; in total, 36.8% of isolates that possessed the ant(6)-Ia gene did not show phenotypic resistance to streptomycin. To a lesser extent, silent genes were also detected in clindamycin and tetracycline. This study confirmed the high susceptibility of S. uberis to penicillins used as first-line antimicrobials for S. uberis mastitis treatment.

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Halasa T., Huijps K., Østerås O., Hogeveen H. Economic effects of bovine mastitis and mastitis management: A review. Vet. Q. 2007;29:18–31. doi: 10.1080/01652176.2007.9695224. PubMed DOI

Bradley A.J., Leach K.A., Breen J.E., Green L.E., Gree M.J. Survey of the incidence and aetiology of mastitis on dairy farms in England and Wales. Vet. Rec. 2007;60:253–257. doi: 10.1136/vr.160.8.253. PubMed DOI

Vezina B., Al-harbi H., Ramay H.R., Soust M., Moore R.J., Olchowy T.W., Alawneh J.I. Sequence characterisation and novel insights into bovine mastitis-associated Streptococcus uberis in dairy herds. Sci. Rep. 2021;11:3046. doi: 10.1038/s41598-021-82357-3. PubMed DOI PMC

Zouharova M., Nedbalcova K., Slama P., Bzdil J., Masarikova M., Matiasovic J. Occurrence of virulence associated genes in Streptococcus uberis and Streptococcus parauberis isolated from bovine mastitis. Vet. Med.-Czech. 2022;67:123–130. doi: 10.17221/95/2021-VETMED. PubMed DOI PMC

Saini V., McClure J.T., Léger D., Dufour S., Sheldon A.G., Scholl D.T., Barkema H.W. Antimicrobial use on Canadian dairy farms. J. Dairy Sci. 2012;95:1209–1221. doi: 10.3168/jds.2011-4527. PubMed DOI

Boonyayatra S. Treatment of bovine mastitis during lactating period. Chiang Mai Vet. J. 2012;10:87–107.

Bolte J., Zhang Y., Wente N., Krömker V. In Vitro Susceptibility of Mastitis Pathogens Isolated from Clinical Mastitis Cases on Northern German Dairy Farms. Vet. Sci. 2020;7:10. doi: 10.3390/vetsci7010010. PubMed DOI PMC

Martins L., Gonçalves J.L., Leite R.F., Tomazi T., Rall V.L.M., Santos M.V. Association between antimicrobial use and antimicrobial resistance of Streptococcus uberis causing clinical mastitis. J. Dairy Sci. 2021;104:12030–12041. doi: 10.3168/jds.2021-20177. PubMed DOI

Zhang T., Niu G., Boonyayatra S., Pichpol D. Antimicrobial Resistance Profiles and Genes in Streptococcus uberis Associated With Bovine Mastitis in Thailand. Front. Vet. Sci. 2021;8:705338. doi: 10.3389/fvets.2021.705338. PubMed DOI PMC

Vezina B., Rosa M.N., Canu A., Tola S. Genomic surveillance reveals antibiotic resistance gene transmission via phage recombinases within sheep mastitis-associated Streptococcus uberis. BMC Vet. Res. 2022;18:264. doi: 10.1186/s12917-022-03341-1. PubMed DOI PMC

de Jong A., Garch F.E., Simjee S., Moyaert H., Rose M., Youala M., Siegwart E. VetPath Study Group. Monitoring of antimicrobial susceptibility of udder pathogens recovered from cases of clinical mastitis in dairy cows across Europe: VetPath results. Vet. Microbiol. 2018;213:73–81. doi: 10.1016/j.vetmic.2017.11.021. PubMed DOI

Constable P.D., Morin D.E. Treatment of clinical mastitis: Using antimicrobial susceptibility profiles for treatment decisions. Vet. Clin. N. Am. Food Anim. Pract. 2003;19:139–155. doi: 10.1016/S0749-0720(02)00068-3. PubMed DOI

Pratova H., Pokludova L., Dubska M., Bures J. Prevalence rezistence k antimikrobikům u vybraných původců mastitidy skotu. Veterinářství. 2021;71:20–31. (In Czech)

Nedbalcova K., Nechvatalova K., Pokludova L., Bures J., Kucerova Z., Koutecka L., Hera A. Resistance to selected beta-lactam antibiotics. Vet. Microbiol. 2014;171:328–336. doi: 10.1016/j.vetmic.2014.02.004. PubMed DOI

Davies P.L., Leigh J.A., Bradley A.J., Archer S.C., Emes R.D., Green M.J. Molecular Epidemiology of Streptococcus uberis Clinical Mastitis in Dairy Herds: Strain Heterogeneity and Transmission. J. Clin. Microbiol. 2016;54:68–74. doi: 10.1128/JCM.01583-15. PubMed DOI PMC

Pokludova L., Maxova L., Maskova Z., Novotna P., Chumchalova J., Bures J. Léčiva používaná k prevenci a terapii mastitid–přehled, trendy spotřeb a důraz na zodpovědnější přístup k antimikrobikům. Medicines used to prevent and treat mastitis–overview, consumption trends and emphasis on a more responsible approach to antimicrobials. Veterinářství. 2021;71:82–93. (In Czech)

Käppeli N., Morach M., Zurfluh K., Corti S., Nüesch-Inderbinen M., Stephan R. Sequence Types and Antimicrobial Resistance Profiles of Streptococcus uberis Isolated from Bovine Mastitis. Front. Vet. Sci. 2019;16:234. doi: 10.3389/fvets.2019.00234. PubMed DOI PMC

Monistero V., Barberio A., Cremonesi P., Castiglioni B., Morandi S., Lassen D.C.K., Astrup L.B., Locatelli C., Piccinini R., Addis M.F., et al. Genotyping and Antimicrobial Susceptibility Profiling of Streptococcus uberis Isolated from a Clinical Bovine Mastitis Outbreak in a Dairy Farm. Antibiotics. 2021;10:644. doi: 10.3390/antibiotics10060644. PubMed DOI PMC

Haenni M., Lupo A., Madec J. Antimicrobial resistance in Streptococcus spp. Microbiol. Spectr. 2018;6:1–25. doi: 10.1128/microbiolspec.ARBA-0008-2017. PubMed DOI

Haenni M., Galofaro L., Ythier M., Giddey M., Majcherczyk P., Moreillon P., Madec J.Y. Penicillin-binding protein gene alterations in Streptococcus uberis isolates presenting decreased susceptibility to penicillin. Antimicrob. Agents Chemother. 2010;54:1140–1145. doi: 10.1128/AAC.00915-09. PubMed DOI PMC

Zhang H., Yang F., Li X.P., Luo J.Y., Wang L., Zhou Y.L., Yan Y., Wang X.R., Li H.S. Detection of antimicrobial resistence and virulence-related genes in Streptococcus uberis and Streptococcus parauberis isolated from clinical bovine mastitis cases in northwestern China. J. Integr. Agric. 2020;19:2784–2791. doi: 10.1016/S2095-3119(20)63185-9. DOI

Tomazi T., Freu G., Alves B.G., de Souza Filho A.F., Heinemann M.B., Veiga Dos Santos M. Genotyping and antimicrobial resistance of Streptococcus uberis isolated from bovine clinical mastitis. PLoS ONE. 2019;14:e0223719. doi: 10.1371/journal.pone.0223719. PubMed DOI PMC

Abd El-Aziz N.K., Ammar A.M., El Damaty H.M., Abd Elkader R.A., Saad H.A., El-Kazzaz W., Khalifa E. Environmental Streptococcus uberis Associated with Clinical Mastitis in Dairy Cows: Virulence Traits, Antimicrobial and Biocide Resistance, and Epidemiological Typing. Animals. 2021;11:1849. doi: 10.3390/ani11071849. PubMed DOI PMC

EUCAST European Committee on Antimicrobial Susceptibility Testing. Breakpoint Tables for Interpretation of MICs and Zone Diameters. 2022. [(accessed on 5 May 2023)]. Version 12.0. Available online: http://www.eucast.org.

Haenni M., Saras E., Chaussière S., Treilles M., Madec J.Y. ermB mediated erythromycin resistance in Streptococcus uberis from bovine mastitis. Vet. J. 2011;189:356–358. doi: 10.1016/j.tvjl.2010.06.021. PubMed DOI

Cheng J., Qu W., Barkema H.W., Nobrega D.B., Gao J., Liu G., De Buck J., Kastelic J.P., Sun H., Han B. Antimicrobial resistance profiles of 5 common bovine mastitis pathogens in large Chinese dairy herds. J. Dairy Sci. 2019;102:2416–2426. doi: 10.3168/jds.2018-15135. PubMed DOI

Minst K., Märtlbauer E., Miller T., Meyer C. Short communication: Streptococcus species isolated from mastitis milk samples in Germany and their resistance to antimicrobial agents. J. Dairy Sci. 2012;95:6957–6962. doi: 10.3168/jds.2012-5852. PubMed DOI

Cameron M., Saab M., Heider L., McClure J.T., Rodriguez-Lecompte J.C., Sanchez J. Antimicrobial susceptibility patterns of environmental streptococci recovered from bovine milk samples in the Maritime provinces of Canada. Front. Vet. Sci. 2016;3:79. doi: 10.3389/fvets.2016.00079. PubMed DOI PMC

Gruet P., Maincent P., Berthelot X., Kaltsatos V. Bovine mastitis and intramammary drug delivery: Review and perspectives. Adv. Drug Deliv. Rev. 2001;50:245–259. doi: 10.1016/S0169-409X(01)00160-0. PubMed DOI

Persson Y., Nyman A.K.J., Grönlund-Andersson U. Etiology and antimicrobial susceptibility of udder pathogens from cases of subclinical mastitis in dairy cows in Sweden. Acta Vet. Scand. 2011;53:36. doi: 10.1186/1751-0147-53-36. PubMed DOI PMC

Tian X.Y., Zheng N., Han R.W., Ho H., Wang J., Wang Y.T., Wang S.Q., Li H.G., Liu H.W., Yu Z.N. Antimicrobial resistence and virulence genes of Streptococcus isolated from dairy cows with mastitis in China. Microb. Pathog. 2019;131:33–39. doi: 10.1016/j.micpath.2019.03.035. PubMed DOI

Stasiak M., Maćkiw E., Kowalska J., Kucharek K., Postupolski J. Silent Genes: Antimicrobial Resistance and Antibiotic Production. Pol. J. Microbiol. 2021;70:421–429. doi: 10.33073/pjm-2021-040. PubMed DOI PMC

CLSI . Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals. 5th ed. Clinical and Laboratory Standards Institute; Wayne, PA, USA: 2020. CLSI supplement VET01S.

CA-SFM-VET . Comité de l’Antibiogramme de la Société Francaise de Microbiologie—Recommandations Vétérinaries. Société Francaise de Microbiologie; Paris, France: 2021. p. 15.

CLSI . Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals: Second Informational Supplement. 4th ed. Clinical and Laboratory Standards Institute; Wayne, PA, USA: 2013. p. 70. CLSI Document VET01-S2.

Magiorakos A.P., Srinivasan A., Carey R.B., Carmeli Y., Falagas M.E., Giske C.G., Harbarth S., Hindler J.F., Kahlmeter G., Olsson-Liljequist B., et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: An international expert proposal for interim standard definitions for acquired resistance. Clin. Microbiol. Infect. 2012;18:268–281. doi: 10.1111/j.1469-0691.2011.03570.x. PubMed DOI

Quijada N.M., Rodríguez-Lázaro D., Eiros J.M., Hernández M. TORMES: An automated pipeline for whole bacterial genome analysis. Bioinformatics. 2019;35:4207–4212. doi: 10.1093/bioinformatics/btz220. PubMed DOI

Bankevich A., Nurk S., Antipov D., Gurevich A., Dvorkin M., Kulikov A.S., Lesin V.M., Nikolenko S.I., Pham S., Prjibelski A.D., et al. SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing. J. Comput. Biol. 2012;19:455–477. doi: 10.1089/cmb.2012.0021. PubMed DOI PMC

Tange O. GNU Parallel-The Command-Line Power Tool. USENIX Mag. 2011;36:42–47.

Wood D.E., Lu J., Langmead B. Improved metagenomic analysis with Kraken 2. Genome Biol. 2019;20:257. doi: 10.1186/s13059-019-1891-0. PubMed DOI PMC

Zankari E., Hasman H., Cosentino S., Vestergaard M., Rasmussen S., Lund O., Aarestrup F.M., Larsen M.V. Identification of acquired antimicrobial resistance genes. J. Antimicrob. Chemother. 2012;67:2640–2644. doi: 10.1093/jac/dks261. PubMed DOI PMC

McArthur A.G., Waglechner N., Nizam F., Yan A., Azad M.A., Baylay A.J., Bhullar K., Canova M.J., De Pascale G., Ejim L., et al. The comprehensive antibiotic resistance database. Antimicrob. Agents Chemother. 2013;57:3348–3357. doi: 10.1128/AAC.00419-13. PubMed DOI PMC

Gupta S.K., Padmanabhan B.R., Diene S.M., Lopez-Rojas R., Kempf M., Landraud L., Rolain J.M. ARG-ANNOT, a new bioinformatic tool to discover antibiotic resistance genes in bacterial genomes. Antimicrob. Agents Chemother. 2014;58:212–220. doi: 10.1128/AAC.01310-13. PubMed DOI PMC

Seemann T. ABRicate Github. [(accessed on 8 June 2021)]. Available online: https://github.com/tseemann/abricate.

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