Antimicrobial susceptibility of mycoplasma bovis isolates from veal, dairy and beef herds

Epidemiological cut-off methods; Gamithromycin; Genomic clusters; Iterative statistical method; Normalized resistance interpretation; Visual estimation

Abstract :

[en] Mycoplasma bovis is an important pathogen causing mostly pneumonia in calves and mastitis in dairy cattle. In the absence of an effective vaccine, antimicrobial therapy remains the main control measure. Antimicrobial use in veal calves is substantially higher than in conventional herds, but whether veal calves also harbor more resistant M. bovis strains is currently unknown. Therefore, we compared antimicrobial susceptibility test results of M. bovis isolates from different cattle sectors and genomic clusters. The minimum inhibitory concentration of nine antimicrobials was determined for 141 Belgian M. bovis isolates (29 dairy, 69 beef, 12 mixed, 31 veal farms), and was used to estimate the epidemiological cut-off. Acquired resistance was frequently observed for the macrolides, while no acquired resistance to oxytetracycline and doxycycline, minimal acquired resistance to florfenicol and tiamulin, and a limited acquired resistance to enrofloxacin was seen. M. bovis isolates from beef cattle or genomic cluster III had higher odds of being gamithromycin-resistant than those from dairy cattle or genomic clusters IV and V. In this study, no cattle industry could be identified as source of resistant M. bovis strains. A single guideline for antimicrobial use for M. bovis infections, with a small remark for gamithromycin, is likely sufficient. © 2020 by the authors. Licensee MDPI, Basel, Switzerland.

Disciplines :

Veterinary medicine & animal health

Author, co-author :

Bokma, J.; Department of Large Animal Internal Medicine, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, Merelbeke, 9820, Belgium, Department of Pathology, Bacteriology and Avian Diseases, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, Merelbeke, 9820, Belgium

Gille, Linde ; Université de Liège - ULiège > CVU : pôle ruminants-porcs

De Bleecker, K.; Animal Health Service-Flanders, Industrielaan 29, Torhout, 8820, Belgium

Callens, J.; Animal Health Service-Flanders, Industrielaan 29, Torhout, 8820, Belgium

Haesebrouck, F.; Department of Pathology, Bacteriology and Avian Diseases, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, Merelbeke, 9820, Belgium

Pardon, B.; Department of Large Animal Internal Medicine, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, Merelbeke, 9820, Belgium

Boyen, F.; Department of Pathology, Bacteriology and Avian Diseases, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, Merelbeke, 9820, Belgium

Language :

English

Title :

Antimicrobial susceptibility of mycoplasma bovis isolates from veal, dairy and beef herds

Publication date :

2020

Journal title :

Antibiotics

eISSN :

2079-6382

Publisher :

MDPI AG

Volume :

Issue :

Pages :

1-12

Peer reviewed :

Peer Reviewed verified by ORBi

Name of the research project :

Grant number RF17/6313 (MALDIRESP); DGZ Vlaanderen Veepeiler Project 2018; Hercules project G0H2516N (AUGE/15/05)

Funders :

SPF Santé - Service Public Fédéral Santé publique. Sécurité de la Chaîne alimentaire et Environnement
FWO - Fonds Wetenschappelijk Onderzoek Vlaanderen

Available on ORBi :

since 15 February 2021

Statistics

Number of views

56 (3 by ULiège)

Number of downloads

37 (4 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Calcutt, M.J.; Lysnyansky, I.; Sachse, K.; Fox, L.K.; Nicholas, R.A.J.; Ayling, R.D. Gap analysis of Mycoplasma bovis disease, diagnosis and control: An aid to identify future development requirements. Transbound. Emerg. Dis. 2018, 65, 91–109. [CrossRef]
Maunsell, F.P.; Donovan, G.A. Mycoplasma bovis Infections in Young Calves. Vet. Clin. N. A. Food Anim. Pract. 2009, 25, 139–177. [CrossRef] [PubMed]
Maunsell, F.P.; Woolums, A.R.; Francoz, D.; Rosenbusch, R.F.; Step, D.L.; Wilson, D.J.; Janzen, E.D. Mycoplasma bovis infections in cattle. J. Vet. Intern. Med. 2011, 25, 772–783. [CrossRef] [PubMed]
Gautier-Bouchardon, A.V.; Ferré, S.; Le Grand, D.; Paoli, A.; Gay, E.; Poumarat, F. Overall decrease in the susceptibility of Mycoplasma bovis to antimicrobials over the past 30 years in France. PLoS ONE 2014, 9, e87672. [CrossRef] [PubMed]
Cai, H.Y.; McDowall, R.; Parker, L.; Kaufman, E.I.; Caswell, J.L. Changes in antimicrobial susceptibility profiles of Mycoplasma bovis over time. Can. J. Vet. Res. 2019, 83, 34–41.
Klein, U.; de Jong, A.; Youala, M.; El Garch, F.; Stevenin, C.; Moyaert, H.; Rose, M.; Catania, S.; Gyuranecz, M.; Pridmore, A.; et al. New antimicrobial susceptibility data from monitoring of Mycoplasma bovis isolated in Europe. Vet. Microbiol. 2019, 238. [CrossRef]
García-Galán, A.; Nouvel, L.; Baranowski, E.; Gómez-Martín, A.; Sánchez, A.; Citti, C.; de la Fe, C. Mycoplasma bovis in Spanish cattle herds: Two groups of multiresistant isolates predominate, with one remaining susceptible to fluoroquinolones. Pathogens 2020, 9, 545. [CrossRef]
Jelinski, M.; Kinnear, A.; Gesy, K.; Andrés-Lasheras, S.; Zaheer, R.; Weese, S.; McAllister, T.A. Antimicrobial sensitivity testing of Mycoplasma bovis isolates derived from Western Canadian feedlot cattle. Microorganisms 2020, 8, 124. [CrossRef]
Liu, Y.; Xu, S.; Li, M.; Zhou, M.; Huo, W.; Gao, J.; Liu, G.; Kastelic, J.P.; Han, B. Molecular characteristics and antibiotic susceptibility profiles of Mycoplasma bovis associated with mastitis on dairy farms in China. Prev. Vet. Med. 2020, 182, 105106. [CrossRef]
Heuvelink, A.; Reugebrink, C.; Mars, J. Antimicrobial susceptibility of Mycoplasma bovis isolates from veal calves and dairy cattle in the Netherlands. Vet. Microbiol. 2016, 189, 1–7. [CrossRef]
Becker, C.A.M.; Ambroset, C.; Huleux, A.; Vialatte, A.; Colin, A.; Tricot, A.; Arcangioli, M.; Tardy, F. Monitoring Mycoplasma bovis diversity and antimicrobial susceptibility in calf feedlots undergoing a respiratory disease outbreak. Pathogens 2020, 9, 593. [CrossRef] [PubMed]
Gerchman, I.; Levisohn, S.; Mikula, I.; Lysnyansky, I. In vitro antimicrobial susceptibility of Mycoplasma bovis isolated in Israel from local and imported cattle. Vet. Microbiol. 2009, 137, 268–275. [CrossRef]
Catry, B.; Haesebrouck, F.; De Vliegher, S.; Feyen, B.; Vanrobaeys, M.; Opsomer, G.; Schwarz, S.; De Kruif, A. Variability in acquired resistance of Pasteurella and Mannheimia isolates from the nasopharynx of calves, with particular reference to different herd types. Microb. Drug Resist. 2005, 11, 387–394. [CrossRef] [PubMed]
Dorado-García, A.; Mevius, D.J.; Jacobs, J.J.H.; Van Geijlswijk, I.M.; Mouton, J.W.; Wagenaar, J.A.; Heederik, D.J. Quantitative assessment of antimicrobial resistance in livestock during the course of a nationwide antimicrobial use reduction in the Netherlands. J. Antimicrob. Chemother. 2016, 71, 3607–3619. [CrossRef] [PubMed]
Becker, C.A.M.; Thibault, F.M.; Arcangioli, M.A.; Tardy, F. Loss of diversity within Mycoplasma bovis isolates collected in France from bovines with respiratory diseases over the last 35 years. Infect. Genet. Evol. 2015, 33, 118–126. [CrossRef] [PubMed]
Parker, A.M.; Shukla, A.; House, J.K.; Hazelton, M.S.; Bosward, K.L.; Kokotovic, B.; Sheehy, P.A. Genetic characterization of Australian Mycoplasma bovis isolates through whole genome sequencing analysis. Vet. Microbiol. 2016, 196, 118–125. [CrossRef] [PubMed]
Yair, Y.; Borovok, I.; Mikula, I.; Falk, R.; Fox, L.K.; Gophna, U.; Lysnyansky, I. Genomics-based epidemiology of bovine Mycoplasma bovis strains in Israel. BMC Genom. 2020, 21, 70. [CrossRef]
Bokma, J.; Vereecke, N.; De Bleecker, K.; Callens, J.; Ribbens, S.; Nauwynck, H.; Haesebrouck, F.; Theuns, S.; Boyen, F.; Pardon, B. Phylogenomic analysis of Mycoplasma bovis from Belgian veal, dairy and beef herds. Vet. Res. 2020, 51, 121. [CrossRef]
Vereecke, N.; Bokma, J.; Haesebrouck, F.; Nauwynck, H.; Boyen, F.; Pardon, B.; Theuns, S. High quality genome assemblies of Mycoplasma bovis using a taxon-specific Bonito basecaller for MinION and Flongle long-read nanopore sequencing. BMC Bioinform. 2020, 21. [CrossRef]
Ter Laak, E.A.; Noordergraaf, J.H.; Verschure, M.H. Susceptibilities of Mycoplasma bovis, Mycoplasma dispar and Ureaplasma diversum strains to antimicrobial agents in vitro. Antimicrob. Agents Chemother. 1993, 37, 317–321. [CrossRef]
Rosenbusch, R.F.; Kinyon, J.M.; Apley, M.; Funk, N.D.; Smith, S.; Hoffman, L.J. In vitro antimicrobial inhibition profiles of Mycoplasma bovis isolates recovered from various regions of the United States from 2002 to 2003. J. Vet. Diagn. Investig. 2005, 17, 436–441. [CrossRef] [PubMed]
Sulyok, K.M.; Kreizinger, Z.; Fekete, L.; Jánosi, S.; Schweitzer, N.; Turcsányi, I.; Makrai, L.; Erdélyi, K.; Gyuranecz, M. Phylogeny of Mycoplasma bovis isolates from Hungary based on multi locus sequence typing and multiple-locus variable-number tandem repeat analysis. BMC Vet. Res. 2014, 10, 108. [CrossRef] [PubMed]
Thomas, A.; Nicolas, C.; Dizier, I.; Mainil, J.; Linden, A. Antibiotic susceptibilities of recent isolates of Mycoplasma bovis in Belgium. Vet. Rec. 2003, 153, 428–431. [CrossRef] [PubMed]
Barberio, A.; Flaminio, B.; De Vliegher, S.; Supré, K.; Kromker, V.; Garbarino, C.; Arrigoni, N.; Zanardi, G.; Bertocchi, L.; Gobbo, F.; et al. Short communication: In vitro antimicrobial susceptibility of Mycoplasma bovis isolates identified in milk from dairy cattle in Belgium, Germany, and Italy. J. Dairy Sci. 2016, 99, 6578–6584. [CrossRef] [PubMed]
Lerner, U.; Amram, E.; Ayling, R.D.; Mikula, I.; Gerchman, I.; Harrus, S.; Teff, D.; Yogev, D.; Lysnyansky, I. Acquired resistance to the 16-membered macrolides tylosin and tilmicosin by Mycoplasma bovis. Vet. Microbiol. 2014, 168, 365–371. [CrossRef] [PubMed]
Sulyok, K.M.; Kreizinger, Z.; Wehmann, E.; Lysnyansky, I.; Bányai, K.; Marton, S.; Jerzsele, A.; Rónai, Z.; Turcsányi, I.; Makrai, L.; et al. Mutations associated with decreased susceptibility to seven antimicrobial families in field and laboratory-derived Mycoplasma bovis strains. Antimicrob. Agents Chemother. 2017, 61, e01983-16. [CrossRef]
Stipkovits, L.; Ripley, P.H.; Tenk, M.; Glávits, R.; Molnár, T.; Fodor, L. The efficacy of valnemulin (Econor® ) in the control of disease caused by experimental infection of calves with Mycoplasma bovis. Res. Vet. Sci. 2005, 78, 207–215. [CrossRef]
Gudmundsson, A.; Erlendsdottir, H.; Gottfredsson, M.; Gudmundsson, S. Impact of pH and cationic supplementation on in vitro postantibiotic effect. Antimicrob. Agents Chemother. 1991, 35, 2617–2624. [CrossRef]
Catry, B.; Laevens, H.; Devriese, L.A.; Opsomer, G.; De Kruif, A. Antimicrobial resistance in livestock. J. Vet. Pharmacol. Ther. 2003, 26, 81–93. [CrossRef]
Klein, U.; de Jong, A.; Moyaert, H.; El Garch, F.; Leon, R.; Richard-Mazet, A.; Rose, M.; Maes, D.; Pridmore, A.; Thomson, J.R.; et al. Antimicrobial susceptibility monitoring of Mycoplasma hyopneumoniae and Mycoplasma bovis isolated in Europe. Vet. Microbiol. 2017, 204, 188–193. [CrossRef]
Bokma, J.; Van Driessche, L.; Deprez, P.; Haesebrouck, F.; Vahl, M.; Weesendorp, E.; Deurenberg, R.H.; Pardon, B.; Boyen, F. Rapid identification of Mycoplasma bovis from bovine bronchoalveolar lavage fluid with MALDI-TOF MS after enrichment procedure. J. Clin. Microbiol. 2020, 58, e00004-20. [CrossRef]
Bokma, J.; Pardon, B.; Van Driessche, L.; Gille, L.; Deprez, P.; Haesebrouck, F.; Boyen, F. Optimizing identification of Mycoplasma bovis by MALDI-TOF MS. Res. Vet. Sci. 2019, 125, 185–188. [CrossRef] [PubMed]
Hannan, P.C.T. Guidelines and recommendations for antimicrobial minimum inhibitory concentration (MIC) testing against veterinary Mycoplasma species. Vet. Res. 2000, 31, 373–395. [CrossRef] [PubMed]
EUCAST Reading Guide for Broth Microdilution (Version 2.0). Available online: https://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Disk_test_documents/2020_manuals/Reading_guide_BMD_v_2. 0_2020.pdf (accessed on 17 November 2020).
Toutain, P.L.; Bousquet-Mélou, A.; Damborg, P.; Ferran, A.A.; Mevius, D.; Pelligand, L.; Veldman, K.T.; Lees, P. En Route towards European Clinical breakpoints for veterinary antimicrobial susceptibility testing: A position paper explaining the VetCAST approach. Front. Microbiol. 2017, 8, 2344. [CrossRef] [PubMed]
Turnidge, J.; Paterson, D.L. Setting and revising antibacterial susceptibility breakpoints. Clin. Microbiol. Rev. 2007, 20, 391–408. [CrossRef] [PubMed]
Callens, B.; Dewulf, J.; Kronvall, G.; Catry, B.; Haesebrouck, F.; Boyen, F. Antimicrobial resistance surveillance in Escherichia coli by using normalized resistance interpretation. Vet. Microbiol. 2016, 197, 1–7. [CrossRef] [PubMed]
Turnidge, J.; Kahlmeter, G.; Kronvall, G. Statistical characterisation of bacterial wild-type MIC value distributions and the determination of epidemiological cut-off values. Clin. Microbiol. Infect. 2006, 12, 418–425. [CrossRef]
Kronvall, G. Normalized resistance interpretation as a tool for establishing epidemiological MIC susceptibility breakpoints. J. Clin. Microbiol. 2010, 48, 4445–4452. [CrossRef]
Kumar, S.; Stecher, G.; Li, M.; Knyaz, C.; Tamura, K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 2018, 35, 1547–1549. [CrossRef]