An in vitro evaluation of the effect of antimicrobial treatment on bovine mammary microbiota.
Animals
Cattle
Female
Microbiota
/ drug effects
Mammary Glands, Animal
/ microbiology
Mastitis, Bovine
/ microbiology
Milk
/ microbiology
Bacteria
/ drug effects
Anti-Bacterial Agents
/ pharmacology
Microbial Sensitivity Tests
Drug Resistance, Bacterial
/ drug effects
Anti-Infective Agents
/ pharmacology
RNA, Ribosomal, 16S
/ genetics
Antimicrobial resistance
Bovine milk microbiota
Mastitis
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
07 Aug 2024
07 Aug 2024
Historique:
received:
05
04
2024
accepted:
02
08
2024
medline:
8
8
2024
pubmed:
8
8
2024
entrez:
7
8
2024
Statut:
epublish
Résumé
Antimicrobial-resistant bacteria have been an increasing problem in human medicine and animal husbandry since the introduction of antimicrobials on the market in the 1940s. Over the last decades, efforts to reduce antimicrobial usage in animal husbandry have been shown to limit the development of resistant bacteria. Despite this, antimicrobial-resistant bacteria are still commonly detected and isolated worldwide. In this study, we investigated the presence of antimicrobial-resistant bacteria in bovine milk samples using a multiple approach based on culturing and amplicon sequencing. We first enriched milk samples obtained aseptically from bovine udders in the presence of two antimicrobials commonly used to treat mastitis and then described the resistant microbiota by amplicon sequencing and isolate characterization. Our results show that several commensal species and mastitis pathogens harbor antimicrobial resistance and dominate the enriched microbiota in milk in presence of antimicrobial agents. The use of the two different antimicrobials selected for different bacterial taxa and affected the overall microbial composition. These results provide new information on how different antimicrobials can shape the microbiota which is able to survive and reestablish in the udder and point to the fact that antimicrobial resistance is widely spread also in commensal species.
Identifiants
pubmed: 39112607
doi: 10.1038/s41598-024-69273-y
pii: 10.1038/s41598-024-69273-y
doi:
Substances chimiques
Anti-Bacterial Agents
0
Anti-Infective Agents
0
RNA, Ribosomal, 16S
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
18333Subventions
Organisme : The Norwegian Foundation for Research Levy on Agricultural Products (FFL) and the Norwegian Agricultural Agreement Research Fund (JA)
ID : 267623
Organisme : The Norwegian Research Council
ID : 314733
Organisme : JPI-AMR grant from the Research Council of Norway
ID : 296906
Informations de copyright
© 2024. The Author(s).
Références
Derakhshani, H. et al. Invited review: Microbiota of the bovine udder: Contributing factors and potential implications for udder health and mastitis susceptibility. J. Dairy Sci. 101, 10605–10625 (2018).
pubmed: 30292553
doi: 10.3168/jds.2018-14860
Sharun, K. et al. Advances in therapeutic and managemental approaches of bovine mastitis: A comprehensive review. Vet. Q. 41, 107–136 (2021).
pubmed: 33509059
pmcid: 7906113
doi: 10.1080/01652176.2021.1882713
Winther, A. R. et al. Longitudinal dynamics of the bovine udder microbiota. Animal Microbiome 4, 1–10 (2022).
doi: 10.1186/s42523-022-00177-w
Wang, N. et al. Mechanisms by which mastitis affects reproduction in dairy cow: A review. Reprod. Domest. Anim. 56, 1165–1175 (2021).
pubmed: 34008236
doi: 10.1111/rda.13953
Niedziela, D. A., Murphy, M. P., Grant, J., Keane, O. M. & Leonard, F. C. Clinical presentation and immune characteristics in first-lactation Holstein-Friesian cows following intramammary infection with genotypically distinct Staphylococcus aureus strains. J. Dairy Sci. 103, 8453–8466 (2020).
pubmed: 32622604
doi: 10.3168/jds.2019-17433
Yang, W. et al. Bovine TLR2 and TLR4 properly transduce signals from Staphylococcus aureus and E. coli, but S. aureus fails to both activate NF-κB in mammary epithelial cells and to quickly induce TNFα and interleukin-8 (CXCL8) expression in the udder. Mol. Immunol. 45, 1385–1397 (2008).
pubmed: 17936907
doi: 10.1016/j.molimm.2007.09.004
Suojala, L., Kaartinen, L. & Pyörälä, S. Treatment for bovine Escherichia coli mastitis–an evidence-based approach. J. Vet. Pharmacol. Ther. 36, 521–531 (2013).
pubmed: 23679229
doi: 10.1111/jvp.12057
Oliveira, L. & Ruegg, P. Treatments of clinical mastitis occurring in cows on 51 large dairy herds in Wisconsin. J. Dairy Sci. 97, 5426–5436 (2014).
pubmed: 24997660
doi: 10.3168/jds.2013-7756
Ganda, E. K. et al. Normal milk microbiome is reestablished following experimental infection with Escherichia coli independent of intramammary antibiotic treatment with a third-generation cephalosporin in bovines. Microbiome 5, 1–17 (2017).
doi: 10.1186/s40168-017-0291-5
Smistad, M., Bakka, H. C., Sølverød, L., Jørgensen, H. J. & Wolff, C. Prevalence of udder pathogens in milk samples from Norwegian dairy cows recorded in a national database in 2019 and 2020. Acta Vet. Scand. 65, 19 (2023).
pubmed: 37264425
pmcid: 10234032
doi: 10.1186/s13028-023-00681-2
Statens Legemiddelverk. Terapianbefaling - bruk av antibakterielle midler til matproduserende dyr. < https://legemiddelverket.no/veterinermedisin/terapianbefalinger/bruk-av-antibakterielle-midler-til-matproduserende-dyr/terapianbefalinger-for-storfe > (2022).
Gruet, P., Maincent, P., Berthelot, X. & Kaltsatos, V. Bovine mastitis and intramammary drug delivery: Review and perspectives. Adv. Drug Deliv. Rev. 50, 245–259 (2001).
pubmed: 11500230
doi: 10.1016/S0169-409X(01)00160-0
Belmar-Liberato, R., Gonzalez-Canga, A., Tamame-Martin, P. & Escribano-Salazar, M. Amoxicillin and amoxicillin-clavulanic acid resistance in veterinary medicine–the situation in Europe: A review. Vet. Med. 56, 473 (2011).
doi: 10.17221/3293-VETMED
Rajala-Schultz, P., Nødtvedt, A., Halasa, T. & Persson Waller, K. Prudent use of antibiotics in dairy cows: The Nordic approach to udder health. Front. Vet. Sci. 8, 623998 (2021).
pubmed: 33748209
pmcid: 7973009
doi: 10.3389/fvets.2021.623998
Hillerton, E., Bryan, M., Biggs, A., Berry, E. & Edmondson, P. Time to standardise dry cow therapy terminology. Vet. Record 180, 301–302 (2017).
pubmed: 28336696
doi: 10.1136/vr.j1308
European Centre for Disease Prevention and Control (ECDC), European Food Safety Authority (EFSA) and European Medicines Agency (EMA). Third joint inter-agency report on integrated analysis of consumption of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from humans and food-producing animals in the EU/EEA, JIACRA III. 2016–2018. (2021).
Mulchandani, R., Wang, Y., Gilbert, M. & Van Boeckel, T. P. Global trends in antimicrobial use in food-producing animals: 2020 to 2030. PLoS Global Public Health 3, e0001305 (2023).
pubmed: 36963007
pmcid: 10021213
doi: 10.1371/journal.pgph.0001305
Østerås, O. Helsekortordningen Storfe 2018 - Statistikksamling. https://www.animalia.no/contentassets/36db1ac2b4f14ec9acc74eea3457ce0e/arsrapport_helsekortordningen_-2018.pdf (2019).
Kuehn, J. S. et al. Bacterial community profiling of milk samples as a means to understand culture-negative bovine clinical mastitis. PloS ONE 8, e61959 (2013).
pubmed: 23634219
pmcid: 3636265
doi: 10.1371/journal.pone.0061959
Oikonomou, G. et al. Microbiota of cow’s milk; distinguishing healthy, sub-clinically and clinically diseased quarters. PloS ONE 9, e85904 (2014).
pubmed: 24465777
pmcid: 3896433
doi: 10.1371/journal.pone.0085904
The European Committee on Antimicrobial Susceptibility Testing. Breakpoint tables for interpretation of MICs and zone diameters. Version 13.0,. http://www.eucast.org . (2023).
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. 7, 10 (2020).
pubmed: 31968649
pmcid: 7157569
McDougall, S., Hussein, H. & Petrovski, K. Antimicrobial resistance in Staphylococcus aureus, Streptococcus uberis and Streptococcus dysgalactiae from dairy cows with mastitis. N. Z. Vet. J. 62, 68–76 (2014).
pubmed: 24215609
doi: 10.1080/00480169.2013.843135
Soares, G. M. S. et al. Mechanisms of action of systemic antibiotics used in periodontal treatment and mechanisms of bacterial resistance to these drugs. J. Appl. Oral Sci. 20, 295–309 (2012).
pubmed: 22858695
pmcid: 3881775
doi: 10.1590/S1678-77572012000300002
De Buck, J. et al. Non-aureus staphylococci and bovine udder health: Current understanding and knowledge gaps. Front. Vet. Sci. 8, 658031 (2021).
pubmed: 33937379
pmcid: 8081856
doi: 10.3389/fvets.2021.658031
Andrews, J. M. Determination of minimum inhibitory concentrations. J. Antimicrob. Chemother. 48, 5–16 (2001).
pubmed: 11420333
doi: 10.1093/jac/48.suppl_1.5
EUCAST. Reading Guide for Broth Microdilution, version 4.0. (Eucast.org, 2022).
Nocker, A., Cheung, C.-Y. & Camper, A. K. Comparison of propidium monoazide with ethidium monoazide for differentiation of live vs. dead bacteria by selective removal of DNA from dead cells. J. Microbiol. Methods 67, 310–320 (2006).
pubmed: 16753236
doi: 10.1016/j.mimet.2006.04.015
Casalta, E. & Montel, M.-C. Safety assessment of dairy microorganisms: The Lactococcus genus. Int. J. Food Microbiol. 126, 271–273 (2008).
pubmed: 17976847
doi: 10.1016/j.ijfoodmicro.2007.08.013
Klostermann, K. et al. Intramammary infusion of a live culture of Lactococcus lactis for treatment of bovine mastitis: Comparison with antibiotic treatment in field trials. J. Dairy Res. 75, 365–373 (2008).
pubmed: 18680622
doi: 10.1017/S0022029908003373
Abdi, R. D. et al. Antimicrobial resistance of Staphylococcus aureus isolates from dairy cows and genetic diversity of resistant isolates. Foodborne Pathog. Dis. 15, 449–458 (2018).
pubmed: 29394099
doi: 10.1089/fpd.2017.2362
Cheng, J. et al. Antimicrobial resistance profiles of 5 common bovine mastitis pathogens in large Chinese dairy herds. J. Dairy Sci. 102, 2416–2426 (2019).
pubmed: 30639013
doi: 10.3168/jds.2018-15135
Denamiel, G., Llorente, P., Carabella, M., Rebuelto, M. & Gentilini, E. Anti-microbial susceptibility of Streptococcus spp. isolated from bovine mastitis in Argentina. J. Vet. Med. Ser. B 52, 125–128 (2005).
doi: 10.1111/j.1439-0450.2005.00830.x
Kalayu, A. A. et al. Burden and antimicrobial resistance of S. aureus in dairy farms in Mekelle Northern Ethiopia. BMC Vet. Res. 16, 1–8 (2020).
doi: 10.1186/s12917-020-2235-8
Thomas, V. et al. Antimicrobial susceptibility monitoring of mastitis pathogens isolated from acute cases of clinical mastitis in dairy cows across Europe: VetPath results. Int. J. Antimicrob. Agents 46, 13–20 (2015).
pubmed: 26003836
doi: 10.1016/j.ijantimicag.2015.03.013
Grunwald, L. & Petz, M. Food processing effects on residues: Penicillins in milk and yoghurt. Anal. Chim. Acta 483, 73–79 (2003).
doi: 10.1016/S0003-2670(02)01405-8
Jiménez-Flores, R. & Brisson, G. The milk fat globule membrane as an ingredient: Why, how, when?. Dairy Sci. Technol. 88, 5–18 (2008).
doi: 10.1051/dst:2007005
Ly, M., Vo, N., Le, T., Belin, J.-M. & Waché, Y. Diversity of the surface properties of Lactococci and consequences on adhesion to food components. Colloids Surf. B Biointerfaces 52, 149–153 (2006).
pubmed: 16844359
doi: 10.1016/j.colsurfb.2006.04.015
Brisson, G., Payken, H. F., Sharpe, J. P. & Jiménez-Flores, R. Characterization of Lactobacillus reuteri interaction with milk fat globule membrane components in dairy products. J. Agric. Food Chem. 58, 5612–5619 (2010).
pubmed: 20377223
doi: 10.1021/jf904381s
Bertelloni, F. et al. Detection of genes encoding for enterotoxins, TSST-1, and biofilm production in coagulase-negative staphylococci from bovine bulk tank milk. Dairy Sci. Technol. 95, 341–352 (2015).
doi: 10.1007/s13594-015-0214-9
Turchi, B. et al. Coagulase negative staphylococci from ovine milk: Genotypic and phenotypic characterization of susceptibility to antibiotics, disinfectants and biofilm production. Small Rumin. Res. 183, 106030 (2020).
doi: 10.1016/j.smallrumres.2019.106030
Fišarová, L., Pantůček, R., Botka, T. & Doškař, J. Variability of resistance plasmids in coagulase-negative staphylococci and their importance as a reservoir of antimicrobial resistance. Res. Microbiol. 170, 105–111 (2019).
pubmed: 30503569
doi: 10.1016/j.resmic.2018.11.004
Argudín, M. A., Vanderhaeghen, W. & Butaye, P. Diversity of antimicrobial resistance and virulence genes in methicillin-resistant non-Staphylococcus aureus staphylococci from veal calves. Res. Vet. Sci. 99, 10–16 (2015).
pubmed: 25637268
doi: 10.1016/j.rvsc.2015.01.004
Balaban, N. & Rasooly, A. Analytical chromatography for recovery of small amounts of staphylococcal enterotoxins from food. Int. J. Food Microbiol. 64, 33–40 (2001).
pubmed: 11252509
doi: 10.1016/S0168-1605(00)00439-6
Chen, M. et al. Molecular Mechanism of Staphylococcus xylosus resistance against tylosin and florfenicol. Infect. Drug Resist. https://doi.org/10.2147/IDR.S379264 (2022).
doi: 10.2147/IDR.S379264
pubmed: 36597456
pmcid: 9805726
Raspanti, C. G. et al. Prevalence and antibiotic susceptibility of coagulase-negative Staphylococcus species from bovine subclinical mastitis in dairy herds in the central region of Argentina. Rev. Argent. de Microbiol. 48, 50–56 (2016).
Shin, B. & Park, W. Zoonotic diseases and phytochemical medicines for microbial infections in veterinary science: Current state and future perspective. Front. Vet. Sci. 5, 166 (2018).
pubmed: 30140679
pmcid: 6095004
doi: 10.3389/fvets.2018.00166
Cao, L., Wu, J., Xie, F., Hu, S. & Mo, Y. Efficacy of nisin in treatment of clinical mastitis in lactating dairy cows. J. Dairy Sci. 90, 3980–3985 (2007).
pubmed: 17639009
doi: 10.3168/jds.2007-0153
Ngassam-Tchamba, C. et al. In vitro and in vivo assessment of phage therapy against Staphylococcus aureus causing bovine mastitis. J. Global Antimicrob. Resist. 22, 762–770 (2020).
doi: 10.1016/j.jgar.2020.06.020
Ganda, E. K. et al. Longitudinal metagenomic profiling of bovine milk to assess the impact of intramammary treatment using a third-generation cephalosporin. Sci. Rep. 6, 37565 (2016).
pubmed: 27874095
pmcid: 5118806
doi: 10.1038/srep37565
Porcellato, D., Meisal, R., Bombelli, A. & Narvhus, J. A. A core microbiota dominates a rich microbial diversity in the bovine udder and may indicate presence of dysbiosis. Sci. Rep. 10, 1–14 (2020).
doi: 10.1038/s41598-020-77054-6
Braem, G. et al. Antibacterial activities of coagulase-negative staphylococci from bovine teat apex skin and their inhibitory effect on mastitis-related pathogens. J. Appl. Microbiol. 116, 1084–1093 (2014).
pubmed: 24443828
doi: 10.1111/jam.12447
Woodward, W., Besser, T., Ward, A. & Corbeil, L. In vitro growth inhibition of mastitis pathogens by bovine teat skin normal flora. Can. J. Vet. Res. 51, 27 (1987).
pubmed: 3552170
pmcid: 1255269
Isaac, P. et al. Commensal coagulase-negative Staphylococcus from the udder of healthy cows inhibits biofilm formation of mastitis-related pathogens. Vet. Microbiol. 207, 259–266 (2017).
pubmed: 28757033
doi: 10.1016/j.vetmic.2017.05.025
Bouchard, D. S. et al. Lactic acid bacteria isolated from bovine mammary microbiota: Potential allies against bovine mastitis. PloS ONE 10, e0144831 (2015).
pubmed: 26713450
pmcid: 4694705
doi: 10.1371/journal.pone.0144831
Alharbi, K. N. & Alsaloom, A. N. Characterization of lactic bacteria isolated from raw milk and their antibacterial activity against bacteria as the cause of clinical bovine mastitis. J. Food Qual. 2021, 1–8 (2021).
doi: 10.1155/2021/6466645
Taye, Y., Degu, T., Fesseha, H. & Mathewos, M. Isolation and identification of lactic acid bacteria from cow milk and milk products. Sci. World J. https://doi.org/10.1155/2021/4697445 (2021).
doi: 10.1155/2021/4697445
Furtado, D. N., Todorov, S. D., Landgraf, M., Destro, M. T. & Franco, B. D. Bacteriocinogenic Lactococcus lactis subsp. lactis DF04Mi isolated from goat milk: Characterization of the bacteriocin. Braz. J. Microbiol. 45, 1541–1550 (2014).
pubmed: 25763065
doi: 10.1590/S1517-83822014000400052
Sorge, U. S., Huber-Schlenstedt, R. & Schierling, K. In vitro antimicrobial resistance profiles of Streptococcus uberis, Lactococcus spp., and Enterococcus spp. from quarter milk samples of cows between 2015 and 2019 in Southern Germany. J. Dairy Sci. 104, 5998–6012 (2021).
pubmed: 33685690
doi: 10.3168/jds.2020-19896
Plumed-Ferrer, C. et al. Antimicrobial susceptibilities and random amplified polymorphic DNA-PCR fingerprint characterization of Lactococcus lactis ssp. lactis and Lactococcus garvieae isolated from bovine intramammary infections. J. Dairy Sci. 98, 6216–6225 (2015).
pubmed: 26142865
doi: 10.3168/jds.2015-9579
dos Santos Nascimento, J., Fagundes, P. C., de Paiva Brito, M. A. V., Dos Santos, K. R. N. & de Freire Bastos, Md. C. Production of bacteriocins by coagulase-negative staphylococci involved in bovine mastitis. Vet. Microbiol. 106, 61–71 (2005).
pubmed: 15737474
doi: 10.1016/j.vetmic.2004.10.014
Fuda, C., Fisher, J. & Mobashery, S. β-Lactam resistance in Staphylococcus aureus: The adaptive resistance of a plastic genome. Cell. Mol. Life Sci. 62, 2617–2633 (2005).
pubmed: 16143832
pmcid: 11139134
doi: 10.1007/s00018-005-5148-6
Chambers, H. F. Solving staphylococcal resistance to β-lactams. Trends Microbiol. 11, 145–148 (2003).
pubmed: 12706985
doi: 10.1016/S0966-842X(03)00046-5
Giulieri, S. G. Case commentary: The hidden side of oxacillin resistance in Staphylococcus aureus. Antimicrob. Agents Chemother. 67, e00716-00723 (2023).
pubmed: 37655923
pmcid: 10583679
doi: 10.1128/aac.00716-23
Hess, K. A. et al. Failure of mecA/mecC PCR testing to accurately predict oxacillin resistance in a patient with Staphylococcus aureus infective endocarditis. Antimicrob. Agents Chemother. 67, e00437-00423 (2023).
pubmed: 37341623
pmcid: 10583684
doi: 10.1128/aac.00437-23
Hryniewicz, M. M. & Garbacz, K. Borderline oxacillin-resistant Staphylococcus aureus (BORSA)–a more common problem than expected?. J. Med. Microbiol. 66, 1367–1373 (2017).
pubmed: 28893360
doi: 10.1099/jmm.0.000585
McDougall, S., Clausen, L., Hintukainen, J. & Hunnam, J. Randomized, controlled, superiority study of extended duration of therapy with an intramammary antibiotic for treatment of clinical mastitis. J. Dairy Sci. 102, 4376–4386 (2019).
pubmed: 30879816
doi: 10.3168/jds.2018-15141
MacDiarmid, S. Antibacterial drugs used against mastitis in cattle by the systemic route. N. Z. Vet. J. 26, 290–295 (1978).
pubmed: 284237
doi: 10.1080/00480169.1978.34574
Ajose, D. J. et al. Combating bovine mastitis in the dairy sector in an era of antimicrobial resistance: Ethno-veterinary medicinal option as a viable alternative approach. Front. Vet. Sci. 9, 287 (2022).
doi: 10.3389/fvets.2022.800322
Callahan, B. J. et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016).
pubmed: 27214047
pmcid: 4927377
doi: 10.1038/nmeth.3869
Murali, A., Bhargava, A. & Wright, E. S. IDTAXA: A novel approach for accurate taxonomic classification of microbiome sequences. Microbiome 6, 1–14 (2018).
doi: 10.1186/s40168-018-0521-5
Quast, C. et al. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596 (2012).
pubmed: 23193283
pmcid: 3531112
doi: 10.1093/nar/gks1219
Camacho, C. et al. BLAST+: Architecture and applications. BMC Bioinform. 10, 1–9 (2009).
doi: 10.1186/1471-2105-10-421
Dixon, P. VEGAN, a package of R functions for community ecology. J. Veg. Sci. 14, 927–930 (2003).
doi: 10.1111/j.1654-1103.2003.tb02228.x
Singhal, N., Kumar, M., Kanaujia, P. K. & Virdi, J. S. MALDI-TOF mass spectrometry: An emerging technology for microbial identification and diagnosis. Front. Microbiol. 6, 791 (2015).
pubmed: 26300860
pmcid: 4525378
doi: 10.3389/fmicb.2015.00791