Genotyping and antimicrobial resistance of Streptococcus uberis isolated from bovine clinical mastitis


Autoři: Tiago Tomazi aff001;  Gustavo Freu aff001;  Bruna Gomes Alves aff001;  Antonio Francisco de Souza Filho aff003;  Marcos Bryan Heinemann aff003;  Marcos Veiga dos Santos aff001
Působiště autorů: Department of Animal Production and Nutrition, Milk Quality Research Laboratory (Qualileite), University of São Paulo, Pirassununga, Brazil aff001;  Department of Population Medicine and Diagnostic Sciences, School of Veterinary Medicine, Cornell University, Ithaca, New York, United States of America aff002;  Department of Preventive Veterinary Medicine and Animal Health, Laboratory of Bacterial Zoonosis, University of São Paulo, São Paulo, Brazil aff003
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0223719

Souhrn

A genotypic characterization of Streptococcus uberis isolated from clinical mastitis (CM) in dairy cows, and the association of Strep. uberis genotypes and antimicrobial susceptibility (AMS) was performed. A total of 89 isolates identified as Strep. uberis from 86 dairy cows with CM in 17 dairy herds of Southeastern Brazil were genotyped using random amplified polymorphic DNA (RAPD) analysis. After genotyping, two clusters (I and II) were created according to RAPD types. A commercial broth microdilution test was used to determine the susceptibility of Strep. uberis isolates to 8 antimicrobials (ampicillin, ceftiofur, cephalothin, erythromycin, penicillin, penicillin+novobiocin, pirlimycin and tetracycline). For each antimicrobial, we determined the minimal inhibitory concentrations that inhibit 50% (MIC50) and 90% (MIC90) of Strep. uberis strains. Differences in AMS among genotypic clusters were evaluated using mixed regression models. Overall, a great polymorphism (56 RAPD-types) was found among Strep. uberis isolates, although a higher genetic similarity (based on the PCR bands features) was observed within herds after genotypic clustering. No differences in AMS were observed among clusters. Strep. uberis isolated from bovine CM were resistant to most antimicrobials, with the exception of cephalothin and penicillin+novobiocin.

Klíčová slova:

Antimicrobial resistance – Antimicrobials – Bovine mastitis – Mastitis – Penicillin – Streptococcus – Tetracyclines – Random amplified polymorphic DNA technique


Zdroje

1. Ruegg PL. New perspectives in udder health management. Vet Clin North Am Food Anim Pract. 2012;28: 149–163. doi: 10.1016/j.cvfa.2012.03.001 22664200

2. Zadoks RN, Gillespie BE, Barkema HW, Sampimon OC, Oliver SP, Schukken YH. Clinical, epidemiological and molecular characteristics of Streptococcus uberis infections in dairy herds. Epidemiol Infect. 2003;130: 335–349. doi: 10.1017/s0950268802008221 12729202

3. Rato MG, Bexiga R, Nunes SF, Cavaco LM, Vilela CL, Santos-Sanches I. Molecular epidemiology and population structure of bovine Streptococcus uberis. J Dairy Sci. 2008;91: 4542–4551. doi: 10.3168/jds.2007-0907 19038929

4. Abureema S, Smooker P, Malmo J, Deighton M. Molecular epidemiology of recurrent clinical mastitis due to Streptococcus uberis: evidence of both an environmental source and recurring infection with the same strain. J Dairy Sci. 2014;97: 285–290. doi: 10.3168/jds.2013-7074 24239086

5. Leelahapongsathon K, Schukken YH, Pinyopummintr T, Suriyasathaporn W. Comparison of transmission dynamics between Streptococcus uberis and Streptococcus agalactiae intramammary infections. J Dairy Sci. 2016;99: 1418–1426. doi: 10.3168/jds.2015-9950 26686709

6. Barkema HW, Schukken YH, Lam TJ, Beiboer ML, Benedictus G, Brand A. Management practices associated with the incidence rate of clinical mastitis. J Dairy Sci. 1999;82: 1643–1654. doi: 10.3168/jds.S0022-0302(99)75393-2 10480089

7. Verbeke J, Piepers S, Supre K, De Vliegher S. Pathogen-specific incidence rate of clinical mastitis in Flemish dairy herds, severity, and association with herd hygiene. J Dairy Sci. 2014;97: 6926–6934. doi: 10.3168/jds.2014-8173 25218745

8. Tomazi, T. Etiological and molecular profile of pathogens causing clinical mastitis, and antimicrobial use in dairy herds. Ph.D. Thesis, University of Sao Paulo. 2017. http://www.teses.usp.br/teses/disponiveis/10/10135/tde-19022018-160453/pt-br.php

9. Pol M, Ruegg PL. Treatment practices and quantification of antimicrobial drug usage in conventional and organic dairy farms in Wisconsin. J Dairy Sci. 2007;90: 249–261. doi: 10.3168/jds.S0022-0302(07)72626-7 17183093

10. Saini V, McClure JT, Léger D, Dufour S, Sheldon AG, Scholl DT, et al. Antimicrobial use on Canadian dairy farms. J Dairy Sci. 2012; 95: 1209–1221. doi: 10.3168/jds.2011-4527 22365205

11. Levy SB, Marshall B. Antibacterial resistance worldwide: causes, challenges and responses. Nat Med. 2004;10: 122–129.

12. Van Boeckel TP, Glennon EE, Chen D, Gilbert M, Robinson TP, Grenfell BT, et al. Reducing antimicrobial use in food animals. Science. 2017;357: 1350–1352. doi: 10.1126/science.aao1495 28963240

13. Phuektes P, Mansell PD, Dyson RS, Hooper ND, Dick JS, Browning GF. Molecular epidemiology of Streptococcus uberis isolates from dairy cows with mastitis. J Clin Microbiol. 2001;39: 1460–1466. doi: 10.1128/JCM.39.4.1460-1466.2001 11283072

14. Lopez-Benavides MG, Williamson JH, Pullinger GD, Lacy-Hulbert SJ, Cursons RT, Leigh JA. Field observations on the variation of Streptococcus uberis populations in a pasture-based dairy farm. J Dairy Sci. 2007;90: 5558–5566. doi: 10.3168/jds.2007-0194 18024747

15. Jayarao BM, Oliver SP, Tagg JR, Matthews KR. Genotypic and phenotypic analysis of Streptococcus uberis isolated from bovine mammary secretions. Epidemiol Infect. 1991;107: 543–555. doi: 10.1017/s0950268800049244 1752304

16. Li W, Raoult D, Fournier PE. Bacterial strain typing in the genomic era. FEMS Microbiol Rev. 2009;33: 892–916. doi: 10.1111/j.1574-6976.2009.00182.x 19453749

17. Zadoks RN, Middleton JR, McDougall S, Katholm J, Schukken YH. Molecular epidemiology of mastitis pathogens of dairy cattle and comparative relevance to humans. J Mammary Gland Biol Neoplasia. 2011;16: 357–372. doi: 10.1007/s10911-011-9236-y 21968538

18. Raemy A, Meylan M, Casati S, Gaia V, Berchtold B, Boss R, et al. Phenotypic and genotypic identification of streptococci and related bacteria isolated from bovine intramammary infections. Acta Vet Scand. 2013; 55:53. doi: 10.1186/1751-0147-55-53 23866930

19. Hassan AA, Khan IU, Abdulmawjood A, Lammler C. Evaluation of PCR methods for rapid identification and differentiation of Streptococcus uberis and Streptococcus parauberis. J Clin Microbiol. 2001;39: 1618–1621. doi: 10.1128/JCM.39.4.1618-1621.2001 11283100

20. Tomita T, Meehan B, Wongkattiya N, Malmo J, Pullinger G, Leigh J, Deighton M. Identification of Streptococcus uberis multilocus sequence types highly associated with mastitis. Appl Environ Microbiol. 2008; 74: 114–124. doi: 10.1128/AEM.01373-07 18024686

21. Lundberg A, Nyman AK, Aspan A, Borjesson S, Unnerstad HE, Waller KP. Udder infections with Staphylococcus aureus, Streptococcus dysgalactiae, and Streptococcus uberis at calving in dairy herds with suboptimal udder health. J Dairy Sci. 2016; 99: 2102–2117. doi: 10.3168/jds.2015-9487 26805990

22. Wieliczko RJ, Williamson JH, Cursons RT, Lacy-Hulbert SJ, Woolford MW. Molecular typing of Streptococcus uberis strains isolated from cases of bovine mastitis. J Dairy Sci. 2002;85: 2149–2154. doi: 10.3168/jds.S0022-0302(02)74293-8 12362446

23. Rajala-Schultz PJ, Smith KL, Hogan SJ, Love BC. Antimicrobial susceptibility of mastitis pathogens from first lactation and older cows. Vet Microbiol. 2004;102: 33–42. doi: 10.1016/j.vetmic.2004.04.010 15288925

24. Schmitt-Van de Leemput E, Zadoks RN. Genotypic and phenotypic detection of macrolide and lincosamide resistance in Streptococcus uberis. J Dairy Sci. 2007;90: 5089–5096. doi: 10.3168/jds.2007-0101 17954749

25. Pitkälä A, Koort J, Björkroth J. Identification and antimicrobial resistance of Streptococcus uberis and Streptococcus parauberis isolated from bovine milk samples. J Dairy Sci. 2008;91: 4075–4081. doi: 10.3168/jds.2008-1040 18832235

26. Tomazi T, Ferreira GC, Orsi AM, Goncalves JL, Ospina PA, Nydam DV et al. Association of herd-level risk factors and incidence rate of clinical mastitis in 20 Brazilian dairy herds. Prev Vet Med. 2018; 161: 9–18. doi: 10.1016/j.prevetmed.2018.10.007 30466663

27. Black RA, Taraba JL, Day GB, Damasceno FA, Bewley JM. Compost bedded pack dairy barn management, performance, and producer satisfaction. J Dairy Sci. 2013;96: 8060–8074. 24404593

28. Wenz JR, Garry FB, Barrington GM. Comparison of disease severity scoring systems for dairy cattle with acute coliform mastitis. J Am Vet Med Assoc. 2006;229: 259–262. doi: 10.2460/javma.229.2.259 16842049

29. National Mastitis Council, Laboratory handbook on bovine mastitis. Verona, WI, USA: National Mastitis Council; 1999.

30. Braga PAC, Gonçalves JL, Barreiro JR, Ferreira CR, Tomazi T, Eberlin MN, et al. Rapid identification of bovine mastitis pathogens by MALDI-TOF Mass Spectrometry. Pesq Vet Bras. 2018; 38:586–594.

31. Gallego FJ, Martinez I. Method to improve reliability of random-amplified polymorphic DNA markers. Biotechniques. 1997;23: 663–664. doi: 10.2144/97234bm27 9343689

32. Tomazi T, Souza Filho AF, Heinemann MB, Santos MV. Molecular characterization and antimicrobial susceptibility pattern of Streptococcus agalactiae isolated from clinical mastitis in dairy cattle. Plos One. 2018;13: 1–18.

33. CLSI. Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals; Approved Guideline—Fourth Edition. CLSI document VET01-S2. Wayne, PA: Clinical and Laboratory Standards Institute. 2013.

34. Douglas VL, Fenwick SG, Pfeiffer DU, Williamson NB, Holmes CW. Genomic typing of Streptococcus uberis isolates from cases of mastitis, in New Zealand dairy cows, using pulsed-field gel electrophoresis. Vet Microbiol. 2000;75: 27–41. doi: 10.1016/s0378-1135(00)00184-x 10865150

35. Rato MG, Bexiga R, Florindo C, Cavaco LM, Vilela CL, Santos-Sanches I. Antimicrobial resistance and molecular epidemiology of streptococci from bovine mastitis. Vet Microbiol. 2013;161: 286–294. doi: 10.1016/j.vetmic.2012.07.043 22964008

36. Tabit FT. Advantages and limitations of potential methods for the analysis of bacteria in milk: a review. J Food Sci Technol. 2016; 53: 42–49. doi: 10.1007/s13197-015-1993-y 26787931

37. Rossitto PV, Ruiz L, Kikuchi Y, Glenn K, Luiz K, Watts JL, et al. Antibiotic susceptibility patterns for environmental streptococci isolated from bovine mastitis in central California dairies. J Dairy Sci. 2002;85: 132–138. doi: 10.3168/jds.S0022-0302(02)74061-7 11860105

38. Pol M, Ruegg PL. Relationship between antimicrobial drug usage and antimicrobial susceptibility of gram-positive mastitis pathogens. J Dairy Sci. 2007;90: 262–273. doi: 10.3168/jds.S0022-0302(07)72627-9 17183094

39. Kaczorek E, Malaczewska J, Wojcik R, Rekawek W, Siwicki AK. Phenotypic and genotypic antimicrobial susceptibility pattern of Streptococcus spp. isolated from cases of clinical mastitis in dairy cattle in Poland. J Dairy Sci. 2017;100: 6442–6453. doi: 10.3168/jds.2017-12660 28601447

40. Cameron M, Saab M, Heider L, McClure JT, Rodriguez-Lecompte JC, Sanchez J. Antimicrobial Susceptibility patterns of environmental streptococci recovered from bovine milk samples in the Maritime Provinces of Canada. Front Vet Sci. 2016;3: 1–14.

41. Haenni M, Galofaro L, Ythier M, Giddey M, Majcherczyk P, Moreillon P, Madec JY. 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 20065061


Článek vyšel v časopise

PLOS One


2019 Číslo 10