Extended biofilm susceptibility assay for Staphylococcus aureus bovine mastitis isolates: Evidence for association between genetic makeup and biofilm susceptibility

Journal of Dairy Science

Volumn 94, Issue 12, 2011, Pages 5926-5937

  Melchior, M B ^a,d   van Osch, M H J ^a   Lam, T J G M ^b,c   Vernooij, J C M ^a   Gaastra, W ^a   Fink Gremmels, J ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b GD ANIMAL HEALTH   (Netherlands)

^c Dutch Udder Health Centre   (Netherlands)

^d WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Antimicrobial susceptibility; Bacterial biofilm; Mastitis; Staphylococcus aureus

Indexed keywords

ANTIINFECTIVE AGENT;

ANIMAL; ANIMAL DISEASE; ARTICLE; BACTERIAL GENE; BIOFILM; BOVINE MASTITIS; CATTLE; DRUG EFFECT; FEMALE; GENETICS; ISOLATION AND PURIFICATION; METHODOLOGY; MICROBIOLOGICAL EXAMINATION; MICROBIOLOGY; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION;

ANIMALS; ANTI-BACTERIAL AGENTS; BIOFILMS; CATTLE; FEMALE; GENES, BACTERIAL; MASTITIS, BOVINE; MICROBIAL SENSITIVITY TESTS; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS;

EID: 82155192909     PISSN: 00220302     EISSN: 15253198     Source Type: Journal    
DOI: 10.3168/jds.2011-4243     Document Type: Article

References (52)

1. Amorena B., Gracia E., Monzón M., Leiva J., Oteiza C., Pérez M., Alabart J.-L., Hernández-Yago J. Antibiotic susceptibility assay for Staphylococcus aureus in biofilms developed in vitro. J. Antimicrob. Chemother. 1999, 44:43-55.
2. Barkema H.W., Schukken Y.H., Zadoks R.N. Invited review: The role of cow, pathogen, and treatment regimen in the therapeutic success of bovine Staphylococcus aureus mastitis. J. Dairy Sci. 2006, 89:1877-1895.
3. Bates, D., M. Maechler, and B. Dai. 2008. lme4: Linear mixed-effects models using S4 classes. R package version 0.999375-28. Accessed March 2010. http://lme4.r-forge.r-project.org/.
4. Bradley A.J., Green M.J. Factors affecting cure when treating bovine clinical mastitis with cephalosporin-based intramammary preparations. J. Dairy Sci. 2009, 92:1941-1953.
5. Buzzola F.R., Alvarez L.P., Tuchscherr L.P.N., Barbagelata M.S., Lattar S.M., Calvinho L., Sordelli D.O. Differential abilities of capsulated and noncapsulated Staphylococcus aureus isolates from diverse agr groups to invade mammary epithelial cells. Infect. Immun. 2007, 75:886-891.
6. Ceri H., Olson M.E., Stremick C., Read R.R., Morck D., Buret A. The Calgary Biofilm Device: New technology for rapid determination of antibiotic susceptibilities of bacterial biofilms. J. Clin. Microbiol. 1999, 37:1771-1776.
7. Chan W.C., Coyle B.J., Williams P. Virulence regulation and quorum sensing in staphylococcal infections: Competitive AgrC antagonists as quorum sensing inhibitors. J. Med. Chem. 2004, 47:4633-4641.
8. Costerton J.W., Stewart P.S., Greenberg E.P. Bacterial biofilms: A common cause of persistent infections. Science 1999, 284:1318-1322.
9. Cramton S.E., Gerke C., Schnell N.F., Nichols W.W., Götz F. The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect. Immun. 1999, 67:5427-5433.
10. Deluyker H.A., Chester S.T., Van Oye S.N. A multilocation clinical trial in lactating dairy cows affected with clinical mastitis to compare the efficacy of treatment with intramammary infusions of a lincomycin/neomycin combination with an ampicillin/cloxacillin combination. J. Vet. Pharmacol. Ther. 1999, 22:274-282.
11. Deluyker H.A., Van Oye S.N., Boucher J.F. Factors affecting cure and somatic cell count after pirlimycin treatment of subclinical mastitis in lactating cows. J. Dairy Sci. 2005, 88:604-614.
12. Donlan R.M., Costerton J.W. Biofilms: Survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 2002, 15:167-193.
13. Fox L.K., Zadoks R.N., Gaskins C.T. Biofilm production by Staphylococcus aureus associated with intramammary infection. Vet. Microbiol. 2005, 107:295-299.
14. Giguère S., Prescott J.F., Baggot J.D., Walker R.D., Dowling P.M. Antimicrobial therapy in Veterinary Medicine 2006, Blackwell Publishing, Oxford, UK. 4th.
15. Gilot P., Lina G., Cochard T., Poutrel B. Analysis of the genetic variability of genes encoding the RNA III-activating components Agr and TRAP in a population of Staphylococcus aureus strains isolated from cows with mastitis. J. Clin. Microbiol. 2002, 40:4060-4067.
16. Hasman H., Moodley A., Guardabassi L., Stegger M., Skov R.L., Aarestrup F.M. spa type distribution in Staphylococcus aureus originating from pigs, cattle and poultry. Vet. Microbiol. 2010, 141:326-331.
17. Haveri M., Roslöf A., Rantala L., Pyörälä S. Virulence genes of bovine Staphylococcus aureus from persistent and nonpersistent intramammary infections with different clinical characteristics. J. Appl. Microbiol. 2007, 103:993-1000.
18. Haveri M., Taponen S., Vuopio-Varkila J., Salmenlinna S., Pyörälä S. Bacterial genotype affects the manifestation and persistence of bovine Staphylococcus aureus intramammary infection. J. Clin. Microbiol. 2005, 43:959-961.
19. Høiby N., Bjarnsholt T., Givskov M., Molin S., Ciofu O. Antibiotic resistance of bacterial biofilms. Int. J. Antimicrob. Agents 2010, 35:322-332.
20. Jarraud S., Mougel C., Thioulouse J., Lina G., Meugnier H., Forey F., Nesme X., Etienne J., Vandenesch F. Relationships between Staphylococcus aureus genetic background, virulence factors, agr groups (alleles), and human disease. Infect. Immun. 2002, 70:631-641.
21. Ji G., Beavis R., Novick R.P. Bacterial interference caused by autoinducing peptide variants. Science 1997, 276:2027-2030.
22. Lyon G.J., Wright J.S., Muir T.W., Novick R.P. Key determinants of receptor activation in the agr autoinducing peptides of Staphylococcus aureus. Biochemistry 2002, 41:10095-10104.
23. Mah T.-F.C., O'Toole G.A. Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol. 2001, 9:34-39.
24. MARAN. 2003-2007. MARAN: Monitoring of Antimicrobial Resistance and Antibiotic usage in Animals in the Netherlands in 2003, 2004, 2005, and 2006/2007. CVI-Lelystad, the Netherlands. http://www.cvi.wur.nl/.
25. MARAN. 2005. MARAN-2005: Monitoring of Antimicrobial Resistance and Antibiotic Usage in Animals in the Netherlands in 2005. CIDC-Lelystad, the Netherlands. http://www.cidc-lelystad.nl/.
26. Melchior, M. B. 2007. Biofilms: Implications for the therapy of bovine Staphylococcus aureus mastitis. PhD Thesis. University of Utrecht, Utrecht, the Netherlands.
27. Melchior M.B., Fink-Gremmels J., Gaastra W. Comparative assessment of the antimicrobial susceptibility of Staphylococcus aureus isolates from bovine mastitis in biofilm versus planktonic culture. J. Vet. Med. B Infect. Dis. Vet. Public Health 2006, 53:326-332.
28. Melchior M.B., Fink-Gremmels J., Gaastra W. Extended antimicrobial susceptibility assay for Staphylococcus aureus isolates from bovine mastitis growing in biofilms. Vet. Microbiol. 2007, 125:141-149.
29. Melchior M.B., Vaarkamp H., Fink-Gremmels J. Biofilms: A role in recurrent mastitis infections?. Vet. J. 2006, 171:398-407.
30. Melchior M.B., van Osch M.H., Graat R.M., van Duijkeren E., Mevius D.J., Nielen M., Gaastra W., Fink-Gremmels J. Biofilm formation and genotyping of Staphylococcus aureus bovine mastitis isolates: Evidence for lack of penicillin-resistance in Agr-type II strains. Vet. Microbiol. 2009, 137:83-89.
31. Monzón M., Oteiza C., Leiva J., Amorena B. Synergy of different antibiotic combinations in biofilms of Staphylococcus epidermidis. J. Antimicrob. Chemother. 2001, 48:793-801.
32. O'Gara J.P. ica and beyond: Biofilm mechanisms and regulation in Staphylococcus epidermidis and Staphylococcus aureus. FEMS Microbiol. Lett. 2007, 270:179-188.
33. Oliver S.P., Gillespie B.E., Headrick S.J., Moorehead H., Lunn P., Dowlen H.H., Johnson D.L., Lamar K.C., Chester S.T., Moseley W.M. Efficacy of extended ceftiofur intramammary therapy for treatment of subclinical mastitis in lactating dairy cows. J. Dairy Sci. 2004, 87:2393-2400.
34. Olsen J.E., Christensen H., Aarestrup F.M. Diversity and evolution of blaZ from Staphylococcus aureus and coagulase-negative staphylococci. J. Antimicrob. Chemother. 2006, 57:450-460.
35. Olson M.E., Ceri H., Morck D.W., Buret A.G., Read R.R. Biofilm bacteria: Formation and comparative susceptibility to antibiotics. Can. J. Vet. Res. 2002, 66:86-92.
36. Owens W.E., Ray C.H., Watts J.L., Yancey R.J. Comparison of success of antibiotic therapy during lactation and results of antimicrobial susceptibility tests for bovine mastitis. J. Dairy Sci. 1997, 80:313-317.
37. Pyörälä S.H.K., Pyörälä E.O. Efficacy of parenteral administration of three antimicrobial agents in treatment of clinical mastitis in lactating cows: 487 cases (1989-1995). J. Am. Vet. Med. Assoc. 1998, 212:407-412.
38. Rabello R.F., Moreira B.M., Lopes R.M.M., Teixeira L.M., Riley L.W., Castro A.C. Multilocus sequence typing of Staphylococcus aureus isolates recovered from cows with mastitis in Brazilian dairy herds. J. Med. Microbiol. 2007, 56:1505-1511.
39. Sidhu M.S., Heir E., Leegaard T., Wiger K., Holck A. Frequency of disinfectant resistance genes and genetic linkage with β-lactamase transposon Tn552 among clinical staphylococci. Antimicrob. Agents Chemother. 2002, 46:2797-2803.
40. Smith E.M., Green L.E., Medley G.F., Bird H.E., Fox L.K., Schukken Y.H., Kruze J.V., Bradley A.J., Zadoks R.N., Dowson C.G. Multilocus sequence typing of intercontinental bovine Staphylococcus aureus isolates. J. Clin. Microbiol. 2005, 43:4737-4743.
41. Sol J., Sampimon O.C., Barkema H.W., Schukken Y.H. Factors associated with cure after therapy of clinical mastitis caused by Staphylococcus aureus. J. Dairy Sci. 2000, 83:278-284.
42. Sol J., Sampimon O.C., Snoep J.J., Schukken Y.H. Factors associated with bacteriological cure during lactation after therapy for subclinical mastitis caused by Staphylococcus aureus. J. Dairy Sci. 1997, 80:2803-2808.
43. Stewart P.S. Mechanisms of antibiotic resistance in bacterial biofilms. Int. J. Med. Microbiol. 2002, 292:107-113.
44. Taponen S., Dredge K., Henriksson B., Pyyhtiä A.-M., Suojala L., Junni R., Heinonen K., Pyörälä S. Efficacy of intramammary treatment with procaine penicillin G vs. procaine penicillin G plus neomycin in bovine clinical mastitis caused by penicillin-susceptible, gram-positive bacteria-A double blind field study. J. Vet. Pharmacol. Ther. 2003, 26:193-198.
45. Taponen S., Jantunen A., Pyörälä E., Pyörälä S. Efficacy of targeted 5-day combined parenteral and intramammary treatment of clinical mastitis caused by penicillin-susceptible or penicillin-resistant Staphylococcus aureus. Acta Vet. Scand. 2003, 44:53-62.
46. R Development Core Team. 2008. R: A language and environment for statistical computing. Accessed March 2010. R. Foundations for Statistical Computing, Vienna, Austria. http://www.r-project.org/.
47. Tré-Hardy M., Traore H., El Manssouri N., Vanderbist F., Vaneechoutte M., Devleeschouwer M.J. Evaluation of long-term co-administration of tobramycin and clarithromycin in a mature biofilm model of cystic fibrosis clinical isolates of Pseudomonas aeruginosa. Int. J. Antimicrob. Agents 2009, 34:370-374.
48. van den Borne B.H.P., Nielen M., van Schaik G., Melchior M.B., Lam T.J.G.M., Zadoks R.N. Host adaptation of bovine Staphylococcus aureus seems associated with bacteriological cure after lactational antimicrobial treatment. J. Dairy Sci. 2010, 93:2550-2558.
49. van den Borne B.H.P., van Schaik G., Lam T.J.G.M., Nielen M. Therapeutic effects of antimicrobial treatment during lactation of recently acquired bovine subclinical mastitis: Two linked randomized field trials. J. Dairy Sci. 2010, 93:218-233.
50. Vasudevan P., Nair M.K., Annamalai T., Venkitanarayanan K.S. Phenotypic and genotypic characterization of bovine mastitis isolates of Staphylococcus aureus for biofilm formation. Vet. Microbiol. 2003, 92:179-185.
51. Ziebuhr W., Krimmer V., Rachid S., Lössner I., Götz F., Hacker J. A novel mechanism of phase variation of virulence in Staphylococcus epidermidis: Evidence for control of the polysaccharide intercellular adhesin synthesis by alternating insertion and excision of the insertion sequence element IS256. Mol. Microbiol. 1999, 32:345-356.
52. Ziv G., Storper M. Intramuscular treatment of subclinical staphylococcal mastitis in lactating cows with penicillin G, methicillin and their esters. J. Vet. Pharmacol. Ther. 1985, 8:276-283.