Advertisement

Bovine Mastitis and Biofilms

  • Marielle B. MelchiorEmail author
Chapter
Part of the Springer Series on Biofilms book series (BIOFILMS, volume 6)

Abstract

Biofilm formation in bovine mastitis Staphylococcus aureus isolates was studied since the beginnings of biofilm research, even before the name “biofilm” was actually invented. Compared to other major bovine mastitis pathogens, such as E. coli and Streptococcus uberis relatively much research information is available on S. aureus biofilm formation, biofilm antimicrobial susceptibility and the role of several biofilm related genes. Recent research on biofilm formation from E. coli and Str. uberis shed an interesting light on the whole dynamic process of bacterial invasion, adherence, persistence and evasive strategies of these bacteria, and reveal parallels and differences between these bacteria and S. aureus. In this chapter we present the current knowledge on biofilm formation in the bovine udder as an holistic and dynamic process, with more or less strain specific adaptive strategies and mechanisms which all support perseverance and survival of these bacterial species under stressful circumstances.

Keywords

Hyaluronic Acid Capsular Polysaccharide Bovine Mastitis Milk Whey Aureus Mastitis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Almeida RA, Oliver SP (1993a) Antiphagocytic effect of the capsule of Streptococcus uberis. Zentralbl Veterinärmed B 40(9–10):707–714PubMedGoogle Scholar
  2. Almeida RA, Oliver SP (1993b) Growth curve, capsule expression and characterization of the capsular material of selected strains of Streptococcus uberis. Zentralbl Veterinärmed B 40(9–10):697–706PubMedGoogle Scholar
  3. Almeida RA, Oliver SP (2001) Role of collagen in adherence of Streptococcus uberis to bovine mammary epithelial cells. J Vet Med B Infect Dis Vet Public Health 48(10):759–763PubMedGoogle Scholar
  4. Almeida RA, Luther DA, Kumar SJ, Calvinho LF, Bronze MS, Oliver SP (1996) Adherence of Streptococcus uberis to bovine mammary epithelial cells and to extracellular matrix proteins. Zentralbl Veterinärmed B 43(7):385–392PubMedGoogle Scholar
  5. Almeida RA, Fang W, Oliver SP (1999a) Adherence and internalization of Streptococcus uberis to bovine mammary epithelial cells are mediated by host cell proteoglycans. FEMS Microbiol Lett 177(2):313–317PubMedCrossRefGoogle Scholar
  6. Almeida RA, Luther DA, Oliver SP (1999b) Incubation of Streptococcus uberis with extracellular matrix proteins enhances adherence to and internalization into bovine mammary epithelial cells. FEMS Microbiol Lett 178(1):81–85PubMedCrossRefGoogle Scholar
  7. Almeida RA, Luther DA, Nair R, Oliver SP (2003) Binding of host glycosaminoglycans and milk proteins: possible role in the pathogenesis of Streptococcus uberis mastitis. Vet Microbiol 94(2):131–141PubMedCrossRefGoogle Scholar
  8. Almeida RA, Luther DA, Park HM, Oliver SP (2006) Identification, isolation, and partial characterization of a novel Streptococcus uberis adhesion molecule (SUAM). Vet Microbiol 115(1–3):183–191PubMedCrossRefGoogle Scholar
  9. Amorena B, Gracia E, Monzon M, Leiva J, Oteiza C, Perez M, Alabart JL, Hernandez-Yago J (1999) Antibiotic susceptibility assay for Staphylococcus aureus in biofilms developed in vitro. J Antimicrob Chemother 44(1):43–55PubMedCrossRefGoogle Scholar
  10. Anderson GG, Palermo JJ, Schilling JD, Roth R, Heuser J, Hultgren SJ (2003) Intracellular bacterial biofilm-like pods in urinary tract infections. Science 301(5629):105–107PubMedCrossRefGoogle Scholar
  11. Anderson GG, Goller CC, Justice S, Hultgren SJ, Seed PC (2010) Polysaccharide capsule and sialic acid-mediated regulation promote biofilm-like intracellular bacterial communities during cystitis. Infect Immun 78(3):963–975PubMedCrossRefGoogle Scholar
  12. Apparao MD, Ruegg PL, Lago A, Godden S, Bey R, Leslie K (2009) Relationship between in vitro susceptibility test results and treatment outcomes for gram-positive mastitis pathogens following treatment with cephapirin sodium. J Dairy Sci 92(6):2589–2597PubMedCrossRefGoogle Scholar
  13. Arciola CR, Baldassarri L, Montanaro L (2001) Presence of icaA and icaD genes and slime production in a collection of staphylococcal strains from catheter-associated infections. J Clin Microbiol 39(6):2151–2156PubMedCrossRefGoogle Scholar
  14. Arciola CR, Baldassarri L, Montanaro L (2002) In catheter infections by Staphylococcus epidermidis the intercellular adhesion (ica) locus is a molecular marker of the virulent slime-producing strains. J Biomed Mater Res 59(3):557–562PubMedCrossRefGoogle Scholar
  15. Arnqvist A, Olsen A, Pfeifer J, Russell DG, Normark S (1992) The Crl protein activates cryptic genes for curli formation and fibronectin binding in Escherichia coli HB101. Mol Microbiol 6(17):2443–2452PubMedCrossRefGoogle Scholar
  16. Barkema HW, Schukken YH, Zadoks RN (2006) The role of cow, pathogen, and treatment regimen in the therapeutic success of bovine Staphylococcus aureus mastitis. J Dairy Sci 89(6):1877–1895PubMedCrossRefGoogle Scholar
  17. Barnhart MM, Chapman MR (2006) Curli biogenesis and function. Annu Rev Microbiol 60:131–147PubMedCrossRefGoogle Scholar
  18. Baselga R, Albizu I, De La Cruz M, Del Cacho E, Barberan M, Amorena B (1993) Phase variation of slime production in Staphylococcus aureus: implications in colonization and virulence. Infect Immun 61(11):4857–4862PubMedGoogle Scholar
  19. Baselga R, Albizu I, Amorena B (1994) Staphylococcus aureus capsule and slime as virulence factors in ruminant mastitis. A review. Vet Microbiol 39(3–4):195–204PubMedCrossRefGoogle Scholar
  20. Blum S, Heller ED, Krifucks O, Sela S, Hammer-Muntz O, Leitner G (2008) Identification of a bovine mastitis Escherichia coli subset. Vet Microbiol 132(1–2):135–148PubMedCrossRefGoogle Scholar
  21. Bradley AJ, Green MJ (2001) Adaptation of Escherichia coli to the bovine mammary gland. J Clin Microbiol 39(5):1845–1849PubMedCrossRefGoogle Scholar
  22. Bradley AJ, Green MJ (2009) Factors affecting cure when treating bovine clinical mastitis with cephalosporin-based intramammary preparations. J Dairy Sci 92(5):1941–1953PubMedCrossRefGoogle Scholar
  23. Calzolari A, Giraudo JA, Rampone H, Odierno L, Giraudo AT, Frigerio C, Bettera S, Raspanti C, Hernandez J, Wehbe M, Mattea M, Ferrari M, Larriestra A, Nagel R (1997) Field trials of a vaccine against bovine mastitis. 2. Evaluation in two commercial dairy herds. J Dairy Sci 80(5):854–858PubMedCrossRefGoogle Scholar
  24. Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284(5418):1318–1322PubMedCrossRefGoogle Scholar
  25. Cramton SE, Gerke C, Schnell NF, Nichols WW, Gotz F (1999) The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect Immun 67(10):5427–5433PubMedGoogle Scholar
  26. Cucarella C, Solano C, Valle J, Amorena B, Lasa I, Penades JR (2001) Bap, a Staphylococcus aureus surface protein involved in biofilm formation. J Bacteriol 183(9):2888–2896PubMedCrossRefGoogle Scholar
  27. Dogan B, Klaessig S, Rishniw M, Almeida RA, Oliver SP, Simpson K, Schukken YH (2006) Adherent and invasive Escherichia coli are associated with persistent bovine mastitis. Vet Microbiol 116(4):270–282PubMedCrossRefGoogle Scholar
  28. Dopfer D, Barkema HW, Lam TJ, Schukken YH, Gaastra W (1999) Recurrent clinical mastitis caused by Escherichia coli in dairy cows. J Dairy Sci 82(1):80–85PubMedCrossRefGoogle Scholar
  29. Dopfer D, Almeida RA, Lam TJ, Nederbragt H, Oliver SP, Gaastra W (2000) Adhesion and invasion of Escherichia coli from single and recurrent clinical cases of bovine mastitis in vitro. Vet Microbiol 74(4):331–343PubMedCrossRefGoogle Scholar
  30. Dorr T, Vulic M, Lewis K (2010) Ciprofloxacin causes persister formation by inducing the TisB toxin in Escherichia coli. PLoS Biol 8(2):e1000317PubMedCrossRefGoogle Scholar
  31. Douglas VL, Fenwick SG, Pfeiffer DU, Williamson NB, Holmes CW (2000) Genomic typing of Streptococcus uberis isolates from cases of mastitis, in New Zealand dairy cows, using pulsed-field gel electrophoresis. Vet Microbiol 75(1):27–41PubMedCrossRefGoogle Scholar
  32. Fang W, Almeida RA, Oliver SP (2000) Effects of lactoferrin and milk on adherence of Streptococcus uberis to bovine mammary epithelial cells. Am J Vet Res 61(3):275–279PubMedCrossRefGoogle Scholar
  33. Ferrieres L, Clarke DJ (2003) The RcsC sensor kinase is required for normal biofilm formation in Escherichia coli K-12 and controls the expression of a regulon in response to growth on a solid surface. Mol Microbiol 50(5):1665–1682PubMedCrossRefGoogle Scholar
  34. Foster TJ, Hook M (1998) Surface protein adhesins of Staphylococcus aureus. Trends Microbiol 6(12):484–488PubMedCrossRefGoogle Scholar
  35. Giraudo JA, Calzolari A, Rampone H, Rampone A, Giraudo AT, Bogni C, Larriestra A, Nagel R (1997) Field trials of a vaccine against bovine mastitis. 1. Evaluation in heifers. J Dairy Sci 80(5):845–853PubMedCrossRefGoogle Scholar
  36. Han HR, Pak S 2nd, Guidry A (2000) Prevalence of capsular polysaccharide (CP) types of Staphylococcus aureus isolated from bovine mastitic milk and protection of S. aureus infection in mice with CP vaccine. J Vet Med Sci 62(12):1331–1333PubMedCrossRefGoogle Scholar
  37. Hensen SM, Pavicic MJ, Lohuis JA, Poutrel B (2000) Use of bovine primary mammary epithelial cells for the comparison of adherence and invasion ability of Staphylococcus aureus strains. J Dairy Sci 83(3):418–429PubMedCrossRefGoogle Scholar
  38. Hoffman LR, D’Argenio DA, MacCoss MJ, Zhang Z, Jones RA, Miller SI (2005) Aminoglycoside antibiotics induce bacterial biofilm formation. Nature 436(7054):1171–1175PubMedCrossRefGoogle Scholar
  39. Kai-Larsen Y, Luthje P, Chromek M, Peters V, Wang X, Holm A, Kadas L, Hedlund KO, Johansson J, Chapman MR, Jacobson SH, Romling U, Agerberth B, Brauner A (2010) Uropathogenic Escherichia coli modulates immune responses and its curli fimbriae interact with the antimicrobial peptide LL-37. PLoS Pathog 6(7):e1001010PubMedCrossRefGoogle Scholar
  40. Lammers A, Nuijten PJ, Smith HE (1999) The fibronectin binding proteins of Staphylococcus aureus are required for adhesion to and invasion of bovine mammary gland cells. FEMS Microbiol Lett 180(1):103–109PubMedCrossRefGoogle Scholar
  41. Le Roux Y, Laurent F, Moussaoui F (2003) Polymorphonuclear proteolytic activity and milk composition change. Vet Res 34(5):629–645PubMedCrossRefGoogle Scholar
  42. Leitner G, Lubashevsky E, Glickman A, Winkler M, Saran A, Trainin Z (2003a) Development of a Staphylococcus aureus vaccine against mastitis in dairy cows. I. Challenge trials. Vet Immunol Immunopathol 93(1–2):31–38PubMedCrossRefGoogle Scholar
  43. Leitner G, Yadlin N, Lubashevsy E, Ezra E, Glickman A, Chaffer M, Winkler M, Saran A, Trainin Z (2003b) Development of a Staphylococcus aureus vaccine against mastitis in dairy cows. II. Field trial. Vet Immunol Immunopathol 93(3–4):153–158PubMedCrossRefGoogle Scholar
  44. Lewis K (2000) Programmed death in bacteria. Microbiol Mol Biol Rev 64(3):503–514PubMedCrossRefGoogle Scholar
  45. Maira-Litran T, Kropec A, Abeygunawardana C, Joyce J, Mark G III, Goldmann DA, Pier GB (2002) Immunochemical properties of the staphylococcal poly-N-acetylglucosamine surface polysaccharide. Infect Immun 70(8):4433–4440PubMedCrossRefGoogle Scholar
  46. Matthews KR, Almeida RA, Oliver SP (1994) Bovine mammary epithelial cell invasion by Streptococcus uberis. Infect Immun 62(12):5641–5646PubMedGoogle Scholar
  47. McDougall S, Parkinson TJ, Leyland M, Anniss FM, Fenwick SG (2004) Duration of infection and strain variation in Streptococcus uberis isolated from cows’ milk. J Dairy Sci 87(7):2062–2072PubMedCrossRefGoogle Scholar
  48. McKenney D, Hubner J, Muller E, Wang Y, Goldmann DA, Pier GB (1998) The ica locus of Staphylococcus epidermidis encodes production of the capsular polysaccharide/adhesin. Infect Immun 66(10):4711–4720PubMedGoogle Scholar
  49. McKenney D, Pouliot KL, Wang Y, Murthy V, Ulrich M, Doring G, Lee JC, Goldmann DA, Pier GB (1999) Broadly protective vaccine for Staphylococcus aureus based on an in vivo-expressed antigen. Science 284(5419):1523–1527PubMedCrossRefGoogle Scholar
  50. McKenney D, Pouliot K, Wang Y, Murthy V, Ulrich M, Doring G, Lee JC, Goldmann DA, Pier GB (2000) Vaccine potential of poly-1-6 beta-d-N-succinylglucosamine, an immunoprotective surface polysaccharide of Staphylococcus aureus and Staphylococcus epidermidis. J Biotechnol 83(1–2):37–44PubMedCrossRefGoogle Scholar
  51. Melchior MB (2007) Biofilms: implications for the therapy of bovine Staphylococcus aureus mastitis. Thesis, University of Utrecht, UtrechtGoogle Scholar
  52. Melchior MB, Fink-Gremmels J, Gaastra W (2006a) 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 53(7):326–332PubMedGoogle Scholar
  53. Melchior MB, Vaarkamp H, Fink-Gremmels J (2006b) Biofilms: a role in recurrent mastitis infections? Vet J 171(3):398–407PubMedCrossRefGoogle Scholar
  54. Melchior MB, Fink-Gremmels J, Gaastra W (2007) Extended antimicrobial susceptibility assay for Staphylococcus aureus isolates from bovine mastitis growing in biofilms. Vet Microbiol 125(1–2):141–149PubMedCrossRefGoogle Scholar
  55. Melchior MB, van Osch MH, Graat RM, van Duijkeren E, Mevius DJ, Nielen M, Gaastra W, Fink-Gremmels J (2009) Biofilm formation and genotyping of Staphylococcus aureus bovine mastitis isolates: evidence for lack of penicillin-resistance in Agr-type II strains. Vet Microbiol 137(1–2):83–89PubMedCrossRefGoogle Scholar
  56. Middleton JR, Luby CD, Adams DS (2009) Efficacy of vaccination against staphylococcal mastitis: a review and new data. Vet Microbiol 134(1–2):192–198PubMedCrossRefGoogle Scholar
  57. O’Brien CN, Guidry AJ, Fattom A, Shepherd S, Douglass LW, Westhoff DC (2000) Production of antibodies to Staphylococcus aureus serotypes 5, 8, and 336 using poly(DL-lactide-co-glycolide) microspheres. J Dairy Sci 83(8):1758–1766PubMedCrossRefGoogle Scholar
  58. O’Gara JP (2007) ica and beyond: biofilm mechanisms and regulation in Staphylococcus epidermidis and Staphylococcus aureus. FEMS Microbiol Lett 270(2):179–188PubMedCrossRefGoogle Scholar
  59. Olsen A, Jonsson A, Normark S (1989) Fibronectin binding mediated by a novel class of surface organelles on Escherichia coli. Nature 338(6217):652–655PubMedCrossRefGoogle Scholar
  60. Owens WE, Ray CH, Watts JL, Yancey RJ (1997) Comparison of success of antibiotic therapy during lactation and results of antimicrobial susceptibility tests for bovine mastitis. J Dairy Sci 80(2):313–317PubMedCrossRefGoogle Scholar
  61. Patel D, Almeida RA, Dunlap JR, Oliver SP (2009) Bovine lactoferrin serves as a molecular bridge for internalization of Streptococcus uberis into bovine mammary epithelial cells. Vet Microbiol 137(3–4):297–301PubMedCrossRefGoogle Scholar
  62. Pellegrino M, Giraudo J, Raspanti C, Odierno L, Bogni C (2010) Efficacy of immunization against bovine mastitis using a Staphylococcus aureus avirulent mutant vaccine. Vaccine 28(28):4523–4528PubMedCrossRefGoogle Scholar
  63. Phuektes P, Mansell PD, Dyson RS, Hooper ND, Dick JS, Browning GF (2001) Molecular epidemiology of Streptococcus uberis isolates from dairy cows with mastitis. J Clin Microbiol 39(4):1460–1466PubMedCrossRefGoogle Scholar
  64. Prenafeta A, March R, Foix A, Casals I, Costa L (2010) Study of the humoral immunological response after vaccination with a Staphylococcus aureus biofilm-embedded bacterin in dairy cows: possible role of the exopolysaccharide specific antibody production in the protection from Staphylococcus aureus induced mastitis. Vet Immunol Immunopathol 134(3–4):208–217PubMedCrossRefGoogle Scholar
  65. Prigent-Combaret C, Vidal O, Dorel C, Lejeune P (1999) Abiotic surface sensing and biofilm-dependent regulation of gene expression in Escherichia coli. J Bacteriol 181(19):5993–6002PubMedGoogle Scholar
  66. Prigent-Combaret C, Brombacher E, Vidal O, Ambert A, Lejeune P, Landini P, Dorel C (2001) Complex regulatory network controls initial adhesion and biofilm formation in Escherichia coli via regulation of the csgD gene. J Bacteriol 183(24):7213–7223PubMedCrossRefGoogle Scholar
  67. Pullinger GD, Coffey TJ, Maiden MC, Leigh JA (2007) Multilocus-sequence typing analysis reveals similar populations of Streptococcus uberis are responsible for bovine intramammary infections of short and long duration. Vet Microbiol 119(2–4):194–204PubMedCrossRefGoogle Scholar
  68. Pyorala SH, Pyorala EO (1998) 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 212(3):407–412PubMedGoogle Scholar
  69. Roy JP, DesCoteaux L, DuTremblay D, Beaudry F, Elsener J (2009) Efficacy of a 5-day extended therapy program during lactation with cephapirin sodium in dairy cows chronically infected with Staphylococcus aureus. Can Vet J 50(12):1257–1262PubMedGoogle Scholar
  70. Sears PM, Smith BS, English PB, Herer PS, Gonzalez RN (1990) Shedding pattern of Staphylococcus aureus from bovine intramammary infections. J Dairy Sci 73(10):2785–2789PubMedCrossRefGoogle Scholar
  71. Sol J, Sampimon OC, Snoep JJ, Schukken YH (1997) Factors associated with bacteriological cure during lactation after therapy for subclinical mastitis caused by Staphylococcus aureus. J Dairy Sci 80(11):2803–2808PubMedCrossRefGoogle Scholar
  72. Sol J, Sampimon OC, Barkema HW, Schukken YH (2000) Factors associated with cure after therapy of clinical mastitis caused by Staphylococcus aureus. J Dairy Sci 83(2):278–284PubMedCrossRefGoogle Scholar
  73. Sordelli DO, Buzzola FR, Gomez MI, Steele-Moore L, Berg D, Gentilini E, Catalano M, Reitz AJ, Tollersrud T, Denamiel G, Jeric P, Lee JC (2000) Capsule expression by bovine isolates of Staphylococcus aureus from Argentina: genetic and epidemiologic analyses. J Clin Microbiol 38(2):846–850PubMedGoogle Scholar
  74. Sutra L, Rainard P, Poutrel B (1990) Phagocytosis of mastitis isolates of Staphylococcus aureus and expression of type 5 capsular polysaccharide are influenced by growth in the presence of milk. J Clin Microbiol 28(10):2253–2258PubMedGoogle Scholar
  75. Tamilselvam B, Almeida RA, Dunlap JR, Oliver SP (2006) Streptococcus uberis internalizes and persists in bovine mammary epithelial cells. Microb Pathog 40(6):279–285PubMedCrossRefGoogle Scholar
  76. Taponen S, Dredge K, Henriksson B, Pyyhtia AM, Suojala L, Junni R, Heinonen K, Pyorala S (2003) 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 26(3):193–198PubMedCrossRefGoogle Scholar
  77. Tollersrud T, Kenny K, Reitz AJ Jr, Lee JC (2000) Genetic and serologic evaluation of capsule production by bovine mammary isolates of Staphylococcus aureus and other Staphylococcus spp. from Europe and the United States. J Clin Microbiol 38(8):2998–3003PubMedGoogle Scholar
  78. Tollersrud T, Zernichow L, Andersen SR, Kenny K, Lund A (2001) Staphylococcus aureus capsular polysaccharide type 5 conjugate and whole cell vaccines stimulate antibody responses in cattle. Vaccine 19(28–29):3896–3903PubMedCrossRefGoogle Scholar
  79. van den Borne BH, Halasa T, van Schaik G, Hogeveen H, Nielen M (2010a) Bioeconomic modeling of lactational antimicrobial treatment of new bovine subclinical intramammary infections caused by contagious pathogens. J Dairy Sci 93(9):4034–4044PubMedCrossRefGoogle Scholar
  80. van den Borne BH, van Schaik G, Lam TJ, Nielen M (2010b) Therapeutic effects of antimicrobial treatment during lactation of recently acquired bovine subclinical mastitis: two linked randomized field trials. J Dairy Sci 93(1):218–233PubMedCrossRefGoogle Scholar
  81. Varhimo E, Varmanen P, Fallarero A, Skogman M, Pyorala S, Iivanainen A, Sukura A, Vuorela P, Savijoki K (2010) Alpha- and beta-casein components of host milk induce biofilm formation in the mastitis bacterium Streptococcus uberis. Vet Microbiol 149(3–4):381–389PubMedGoogle Scholar
  82. Vasudevan P, Nair MK, Annamalai T, Venkitanarayanan KS (2003) Phenotypic and genotypic characterization of bovine mastitis isolates of Staphylococcus aureus for biofilm formation. Vet Microbiol 92(1–2):179–185PubMedCrossRefGoogle Scholar
  83. Vidal O, Longin R, Prigent-Combaret C, Dorel C, Hooreman M, Lejeune P (1998) Isolation of an Escherichia coli K-12 mutant strain able to form biofilms on inert surfaces: involvement of a new ompR allele that increases curli expression. J Bacteriol 180(9):2442–2449PubMedGoogle Scholar
  84. Williams MM, Braun-Howland EB (2003) Growth of Escherichia coli in model distribution system biofilms exposed to hypochlorous acid or monochloramine. Appl Environ Microbiol 69(9):5463–5471PubMedCrossRefGoogle Scholar
  85. Wilson DJ, Gonzalez RN, Case KL, Garrison LL, Grohn YT (1999) Comparison of seven antibiotic treatments with no treatment for bacteriological efficacy against bovine mastitis pathogens. J Dairy Sci 82(8):1664–1670PubMedCrossRefGoogle Scholar
  86. Zadoks RN, Allore HG, Barkema HW, Sampimon OC, Grohn YT, Schukken YH (2001a) Analysis of an outbreak of Streptococcus uberis mastitis. J Dairy Sci 84(3):590–599PubMedCrossRefGoogle Scholar
  87. Zadoks RN, Allore HG, Barkema HW, Sampimon OC, Wellenberg GJ, Grohn YT, Schukkent YH (2001b) Cow- and quarter-level risk factors for Streptococcus uberis and Staphylococcus aureus mastitis. J Dairy Sci 84(12):2649–2663PubMedCrossRefGoogle Scholar
  88. Zadoks RN, Gillespie BE, Barkema HW, Sampimon OC, Oliver SP, Schukken YH (2003) Clinical, epidemiological and molecular characteristics of Streptococcus uberis infections in dairy herds. Epidemiol Infect 130(2):335–349PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2011

Authors and Affiliations

  1. 1.MBM Veterinary ConsultancyHeetenThe Netherlands

Personalised recommendations