Journal of Mammary Gland Biology and Neoplasia

, Volume 16, Issue 4, pp 373–382 | Cite as

Methicillin Resistant S. aureus in Human and Bovine Mastitis

Article

Abstract

Staphylococcus aureus is a ubiquitous organism that causes a variety of diseases including mastitis in cattle and humans. High-level resistance of S. aureus to β-lactams conferred by a mecA gene encoding a modified penicillin binding protein (PBP2a) was first observed in the early 1960’s. These methicillin resistant S. aureus (MRSA) have been responsible for both hospital acquired infections (HA-MRSA) and, more recently, community acquired MRSA (CA-MRSA). A small number of human MRSA mastitis cases and outbreaks in maternity or neonatal units have been reported which are generally the result of CA-MRSA. The establishment of the sequence type 398 (ST398) in farm animals, primarily pigs, in the early 2000’s has provided a reservoir of infection for humans and dairy cattle, particularly in continental Europe, described as livestock-associated MRSA (LA-MRSA). Prior to the emergence of ST398 there were sporadic reports of MRSA in bovine milk and cases of mastitis, often caused by strains from human associated lineages. Subsequently, there have been several reports describing bovine udder infections caused by ST-398 MRSA. Recently, another group of LA-MRSA strains was discovered in humans and dairy cattle in Europe. This group carries a divergent mecA gene and includes a number of S. aureus lineages (CC130, ST425, and CC1943) that were hitherto thought to be bovine-specific but are now also found as carriage or clinical isolates in humans. The emergence of MRSA in dairy cattle may be associated with contact with other host species, as in the case of ST398, or with the exchange of genetic material between S. aureus and coagulase negative Staphylococcus species, which are the most common species associated with bovine intramammary infections and commonly carry antimicrobial resistance determinants.

Keywords

Bovine Mastitis MRSA Staphylococcus aureus 

Abbreviations

PBP

penicillin binding protein

MRSA

methicillin resistant S. aureus

HA-MRSA

hospital acquired MRSA

CA-MRSA

community acquired MRSA

ST

sequence type

LA-MRSA

livestock associated MRSA

CC

clonal complex

SSTI

skin and soft tissue infections

SCC

staphylococcal cassette chromosome

PVL

Panton-Valentin leukocidin

MR-CoNS

methicillin resistant coagulase negative staphylococci

PFGE

pulsed-field gel electrophoresis

MLST

multi-locus sequence typing

VNTR

variable number tandem repeat

MSSA

methicillin susceptible S. aureus

RAPD-PCR

random amplified polymorphic DNA polymerase chain reaction

MRSE

methicillin resistant S. epidermidis

References

  1. 1.
    Aires-De-Sousa M, Parente CE, Vieira-Da-Motta O, Bonna IC, Silva DA, De Lencastre H. Appl Environ Microbiol. 2007;73:3845–9.PubMedCrossRefGoogle Scholar
  2. 2.
    Amir LH, Forster DA, Lumley J, Mclachlan H. BMC Publ Health. 2007;7:62.CrossRefGoogle Scholar
  3. 3.
    Amir LH, Garland SM, Lumley J. BMC Fam Pract. 2006;7:57.PubMedCrossRefGoogle Scholar
  4. 4.
    Argudin MA, Tenhagen BA, Fetsch A, Sachsenroder J, Kasbohrer A, Schroeter A, et al. Appl Environ Microbiol. 2011;77:3052–60.PubMedCrossRefGoogle Scholar
  5. 5.
    Armand-Lefevre L, Ruimy R, Andremont A. Emerg Infect Dis. 2005;11:711–4.PubMedGoogle Scholar
  6. 6.
    Baba T, Takeuchi F, Kuroda M, Yuzawa H, Aoki K, Oguchi A, et al. Lancet. 2002;359:1819–27.PubMedCrossRefGoogle Scholar
  7. 7.
    Behari P, Englund J, Alcasid G, Garcia-Houchins S, Weber SG. Infect Control Hosp Epidemiol. 2004;25:778–80.PubMedCrossRefGoogle Scholar
  8. 8.
    Berglund C, Soderquist B. Clin Microbiol Infect. 2008;14:1048–56.PubMedCrossRefGoogle Scholar
  9. 9.
    Bertrand H, Rosenblood LK. CMAJ. 1991;145:299–306.PubMedGoogle Scholar
  10. 10.
    Bradley AJ, Leach KA, Breen JE, Green LE, Green MJ. Vet Rec. 2007;160:253–7.PubMedCrossRefGoogle Scholar
  11. 11.
    Bratu S, Eramo A, Kopec R, Coughlin E, Ghitan M, Yost R, et al. Emerg Infect Dis. 2005;11:808–13.PubMedGoogle Scholar
  12. 12.
    Cavaco LM, Hasman H, Stegger M, Andersen PS, Skov R, Fluit AC, et al. Antimicrob Agents Chemother. 2010;54:3605–8.PubMedCrossRefGoogle Scholar
  13. 13.
    Craven N, Anderson JC, Wilson CD. Res Vet Sci. 1983;34:266–71.PubMedGoogle Scholar
  14. 14.
    Cuny C, Layer F, Strommenger B, Witte W. PLos One. 2011;6:e24360Google Scholar
  15. 15.
    Cuny C, Strommenger B, Witte W, Stanek C. Microb Drug Resist. 2008;14:307–10.PubMedCrossRefGoogle Scholar
  16. 16.
    De Neeling AJ, Van Den Broek MJ, Spalburg EC, Van Santen-Verheuvel MG, Dam-Deisz WD, Boshuizen HC, et al. Vet Microbiol. 2007;122:366–72.Google Scholar
  17. 17.
    De Oliveira AP, Watts JL, Salmon SA, Aarestrup FM. J Dairy Sci. 2000;83:855–62.PubMedCrossRefGoogle Scholar
  18. 18.
    Devriese LA, Hommez J. Res Vet Sci. 1975;19:23–7.PubMedGoogle Scholar
  19. 19.
    Devriese LA, Van Damme LR, Fameree L. Zentralbl Veterinarmed B. 1972;19:598–605.PubMedCrossRefGoogle Scholar
  20. 20.
    Enright MC, Day NP, Davies CE, Peacock SJ, Spratt BG. J Clin Microbiol. 2000;38:1008–15.PubMedGoogle Scholar
  21. 21.
    Erskine RJ, Walker RD, Bolin CA, Bartlett PC, White DG. J Dairy Sci. 2002;85:1111–8.PubMedCrossRefGoogle Scholar
  22. 22.
    Feil EJ, Cooper JE, Grundmann H, Robinson DA, Enright MC, Berendt T, et al. J Bacteriol. 2003;185:3307–16.PubMedCrossRefGoogle Scholar
  23. 23.
    Fessler A, Scott C, Kadlec K, Ehricht R, Monecke S, Schwarz S. J Antimicrob Chemother. 2010;65:619–25.PubMedCrossRefGoogle Scholar
  24. 24.
    Fessler AT, Billerbeck C, Kadlec K, Schwarz S. J Antimicrob Chemother. 2010;65:1576–82.PubMedCrossRefGoogle Scholar
  25. 25.
    Fitzgerald JR, Sturdevant DE, Mackie SM, Gill SR, Musser JM. Proc Natl Acad Sci U S A. 2001;98:8821–6.PubMedCrossRefGoogle Scholar
  26. 26.
    Foxman B, D’arcy H, Gillespie B, Bobo JK, Schwartz K. Am J Epidemiol. 2002;155:103–14.PubMedCrossRefGoogle Scholar
  27. 27.
    Garcia-Alvarez L, Holden MT, Lindsay H, Webb CR, Brown DF, Curran MD, et al. Lancet Infect Dis. 2011.Google Scholar
  28. 28.
    Graveland H, Wagenaar JA, Heesterbeek H, Mevius D, Van Duijkeren E, Heederik D. PLoS One. 2010;5:e10990.PubMedCrossRefGoogle Scholar
  29. 29.
    Hager WD, Barton JR. Infect Dis Obstet Gynecol. 1996;4:97–101.PubMedCrossRefGoogle Scholar
  30. 30.
    Hallin M, De Mendonca R, Denis O, Lefort A, El Garch F, Butaye P, et al. Infect Genet Evol. 2011;11:290–9.PubMedCrossRefGoogle Scholar
  31. 31.
    Hata E, Katsuda K, Kobayashi H, Uchida I, Tanaka K, Eguchi M. J Clin Microbiol. 2010.Google Scholar
  32. 32.
    Haveri M, Suominen S, Rantala L, Honkanen-Buzalski T, Pyorala S. Vet Microbiol. 2005;106:97–102.PubMedCrossRefGoogle Scholar
  33. 33.
    Herron-Olson L, Fitzgerald JR, Musser JM, Kapur V. PLoS One. 2007;2:e1120.PubMedCrossRefGoogle Scholar
  34. 34.
    Huber H, Giezendanner N, Stephan R, Zweifel C. Zoonoses Public Health. 2011;58:343–9.PubMedCrossRefGoogle Scholar
  35. 35.
    Huber H, Koller S, Giezendanner N, Stephan R, Zweifel C. Euro Surveill 2010;15.Google Scholar
  36. 36.
    Huber H, Ziegler D, Pfluger V, Vogel G, Zweifel C, Stephan R. BMC Vet Res. 2011;7:6.PubMedCrossRefGoogle Scholar
  37. 37.
    Huijsdens XW, Van Dijke BJ, Spalburg E, Van Santen-Verheuvel MG, Heck ME, Pluister GN, et al. Ann Clin Microbiol Antimicrob. 2006;5:26.PubMedCrossRefGoogle Scholar
  38. 38.
    Ikawaty R, Brouwer EC, Jansen MD, Van Duijkeren E, Mevius D, Verhoef J, et al. Vet Microbiol. 2009;136:277–84.PubMedCrossRefGoogle Scholar
  39. 39.
    Ito T, Katayama Y, Asada K, Mori N, Tsutsumimoto K, Tiensasitorn C, et al. Antimicrob Agents Chemother. 2001;45:1323–36.PubMedCrossRefGoogle Scholar
  40. 40.
    Jevons MP, Rolinson GN, Knox R. Br Med J. 1961;1:124–5.CrossRefGoogle Scholar
  41. 41.
    Juhasz-Kaszanyitzky E, Janosi S, Somogyi P, Dan A, Van Der Graaf-Van Bloois L, Van Duijkeren E, et al. Emerg Infect Dis. 2007;13:630–2.PubMedCrossRefGoogle Scholar
  42. 42.
    Kalstone C. Am J Obstet Gynecol. 1989;161:120.PubMedGoogle Scholar
  43. 43.
    Kvist LJ, Larsson BW, Hall-Lord ML, Steen A, Schalen C. Int Breastfeed J. 2008;3:6.PubMedCrossRefGoogle Scholar
  44. 44.
    Kwon NH, Park KT, Moon JS, Jung WK, Kim SH, Kim JM, et al. J Antimicrob Chemother. 2005;56:624–32.PubMedCrossRefGoogle Scholar
  45. 45.
    Lee IW, Kang L, Hsu HP, Kuo PL, Chang CM. Am J Obstet Gynecol. 2010;203(332):e1–6.Google Scholar
  46. 46.
    Lee JH. Appl Environ Microbiol. 2003;69:6489–94.PubMedCrossRefGoogle Scholar
  47. 47.
    Lowder BV, Guinane CM, Ben Zakour NL, Weinert LA, Conway-Morris A, Cartwright RA, et al. Proc Natl Acad Sci U S A. 2009;106:19545–50.PubMedCrossRefGoogle Scholar
  48. 48.
    Maiden MC, Bygraves JA, Feil E, Morelli G, Russell JE, Urwin R, et al. Proc Natl Acad Sci U S A. 1998;95:3140–5.PubMedCrossRefGoogle Scholar
  49. 49.
    Makovec JA, Ruegg PL. J Am Vet Med Assoc. 2003;222:1582–9.PubMedCrossRefGoogle Scholar
  50. 50.
    Matheson I, Aursnes I, Horgen M, Aabo O, Melby K. Acta Obstet Gynecol Scand. 1988;67:723–6.PubMedCrossRefGoogle Scholar
  51. 51.
    Moazzez A, Kelso RL, Towfigh S, Sohn H, Berne TV, Mason RJ. Arch Surg. 2007;142:881–4.PubMedCrossRefGoogle Scholar
  52. 52.
    Monecke S, Coombs G, Shore AC, Coleman DC, Akpaka P, Borg M, et al. PLoS One. 2011;6:e17936.PubMedCrossRefGoogle Scholar
  53. 53.
    Monecke S, Kuhnert P, Hotzel H, Slickers P, Ehricht R. Vet Microbiol. 2007;125:128–40.PubMedCrossRefGoogle Scholar
  54. 54.
    Moon JS, Lee AR, Kang HM, Lee ES, Kim MN, Paik YH, et al. J Dairy Sci. 2007;90:1176–85.PubMedCrossRefGoogle Scholar
  55. 55.
    Nam HM, Kim JM, Lim SK, Jang KC, Jung SC. Res Vet Sci. 2010;88:372–4.PubMedCrossRefGoogle Scholar
  56. 56.
    Nam HM, Lee AL, Jung SC, Kim MN, Jang GC, Wee SH, et al. Foodborne Pathog Dis. 2011;8:231–8.PubMedCrossRefGoogle Scholar
  57. 57.
    Nemati M, Hermans K, Lipinska U, Denis O, Deplano A, Struelens M, et al. Antimicrob Agents Chemother. 2008;52:3817–9.PubMedCrossRefGoogle Scholar
  58. 58.
    Nienhoff U, Kadlec K, Chaberny IF, Verspohl J, Gerlach GF, Schwarz S, et al. J Antimicrob Chemother. 2009;64:660–2.PubMedCrossRefGoogle Scholar
  59. 59.
    Nunes SF, Bexiga R, Cavaco LM, Vilela CL. J Dairy Sci. 2007;90:3242–6.PubMedCrossRefGoogle Scholar
  60. 60.
    Oliveira DC, Wu SW, De Lencastre H. Antimicrob Agents Chemother. 2000;44:1906–10.PubMedCrossRefGoogle Scholar
  61. 61.
    Osterman KL, Rahm VA. J Hum Lact. 2000;16:297–302.PubMedCrossRefGoogle Scholar
  62. 62.
    Petrovski KR, Heuer C, Parkinson TJ, Williamson NB. N Z Vet J. 2009;57:109–15.PubMedCrossRefGoogle Scholar
  63. 63.
    Petzer IM, Karzis J, Watermeyer JC, Van Der Schans TJ, Van Reenen R. J S Afr Vet Assoc. 2009;80:17–22.PubMedGoogle Scholar
  64. 64.
    Prashanth K, Rao KR, Reddy PV, Saranathan R, Makki AR. J Global Infect Dis. 2011;3:115–22.CrossRefGoogle Scholar
  65. 65.
    Rabello RF, Moreira BM, Lopes RM, Teixeira LM, Riley LW, Castro AC. J Med Microbiol. 2007;56:1505–11.PubMedCrossRefGoogle Scholar
  66. 66.
    Reddy P, Qi C, Zembower T, Noskin GA, Bolon M. Emerg Infect Dis. 2007;13:298–301.PubMedCrossRefGoogle Scholar
  67. 67.
    Saiman L, O’keefe M, Graham 3rd PL, Wu F, Said-Salim B, Kreiswirth B, et al. Clin Infect Dis. 2003;37:1313–9.PubMedCrossRefGoogle Scholar
  68. 68.
    Sakwinska O, Morisset D, Madec J-Y, Waldvogel A, Moreillon P, Haenni M. Appl Environ Microbiol. 2011;77:3428–32.PubMedCrossRefGoogle Scholar
  69. 69.
    Sampimon OC, Barkema HW, Berends IM, Sol J, Lam TJ. Vet Microbiol. 2009;134:37–44.PubMedCrossRefGoogle Scholar
  70. 70.
    Sampimon OC, Lam TJ, Mevius DJ, Schukken YH, Zadoks RN. Vet Microbiol. 2011;150:173–9.PubMedCrossRefGoogle Scholar
  71. 71.
    Sawant AA, Gillespie BE, Oliver SP. Vet Microbiol. 2009;134:73–81.PubMedCrossRefGoogle Scholar
  72. 72.
    Schwarz D, Diesterbeck US, Failing K, Konig S, Brugemann K, Zschock M, et al. J Dairy Sci. 2010;93:5716–28.PubMedCrossRefGoogle Scholar
  73. 73.
    Seegers H, Fourichon C, Beaudeau F. Vet Res. 2003;34:475–91.PubMedCrossRefGoogle Scholar
  74. 74.
    Sergio DM, Koh TH, Hsu LY, Ogden BE, Goh AL, Chow PK. J Med Microbiol. 2007;56:1107–9.PubMedCrossRefGoogle Scholar
  75. 75.
    Smith EM, Green LE, Medley GF, Bird HE, Fox LK, Schukken YH, et al. J Clin Microbiol. 2005;43:4737–43.PubMedCrossRefGoogle Scholar
  76. 76.
    Smith TC, Male MJ, Harper AL, Kroeger JS, Tinkler GP, Moritz ED, et al. PLoS One. 2009;4:e4258.PubMedCrossRefGoogle Scholar
  77. 77.
    Smith TC, Pearson N. Vector Borne Zoonotic Dis. 2011;11:327–39.PubMedCrossRefGoogle Scholar
  78. 78.
    Smyth DS, Feil EJ, Meaney WJ, Hartigan PJ, Tollersrud T, Fitzgerald JR, et al. J Med Microbiol. 2009;58:1343–53.PubMedCrossRefGoogle Scholar
  79. 79.
    Sung JM, Lloyd DH, Lindsay JA. Microbiology. 2008;154:1949–59.PubMedCrossRefGoogle Scholar
  80. 80.
    Tenover FC, Arbeit RD, Goering RV, Mickelsen PA, Murray BE, Persing DH, et al. J Clin Microbiol. 1995;33:2233–9.PubMedGoogle Scholar
  81. 81.
    Thomsen AC, Espersen T, Maigaard S. Am J Obstet Gynecol. 1984;149:492–5.PubMedGoogle Scholar
  82. 82.
    Thorberg BM, Kuhn I, Aarestrup FM, Brandstrom B, Jonsson P, Danielsson-Tham ML. Vet Microbiol. 2006;115:163–72.PubMedCrossRefGoogle Scholar
  83. 83.
    Turkyilmaz S, Tekbiyik S, Oryasin E, Bozdogan B. Zoonoses Public Health. 2010;57:197–203.PubMedCrossRefGoogle Scholar
  84. 84.
    Udo EE, Pearman JW, Grubb WB. J Hosp Infect. 1993;25:97–108.PubMedCrossRefGoogle Scholar
  85. 85.
    Van Belkum A, Melles DC, Nouwen J, Van Leeuwen WB, Van Wamel W, Vos MC, et al. Infect Genet Evol. 2009;9:32–47.PubMedCrossRefGoogle Scholar
  86. 86.
    Van Cleef BA, Monnet DL, Voss A, Krziwanek K, Allerberger F, Struelens M, et al. Emerg Infect Dis. 2011;17:502–5.PubMedGoogle Scholar
  87. 87.
    Van Den Borne BH, Nielen M, Van Schaik G, Melchior MB, Lam TJ, Zadoks RN. J Dairy Sci. 2010;93:2550–8.PubMedCrossRefGoogle Scholar
  88. 88.
    Van Den Eede A, Martens A, Lipinska U, Struelens M, Deplano A, Denis O, et al. Vet Microbiol. 2009;133:138–44.PubMedCrossRefGoogle Scholar
  89. 89.
    Van Duijkeren E, Ikawaty R, Broekhuizen-Stins MJ, Jansen MD, Spalburg EC, De Neeling AJ, et al. Vet Microbiol. 2008;126:383–9.Google Scholar
  90. 90.
    Vancraeynest D, Haesebrouck F, Deplano A, Denis O, Godard C, Wildemauwe C, et al. J Vet Med B Infect Dis Vet Public Health. 2006;53:418–22.PubMedCrossRefGoogle Scholar
  91. 91.
    Vanderhaeghen W, Cerpentier T, Adriaensen C, Vicca J, Hermans K, Butaye P. Vet Microbiol. 2010.Google Scholar
  92. 92.
    Voss A, Loeffen F, Bakker J, Klaassen C, Wulf M. Emerg Infect Dis. 2005;11:1965–6.PubMedGoogle Scholar
  93. 93.
    Wagenaar JA, Yue H, Pritchard J, Broekhuizen-Stins M, Huijsdens X, Mevius DJ, et al. Vet Microbiol. 2009;139:405–9.PubMedCrossRefGoogle Scholar
  94. 94.
    Wielders CL, Vriens MR, Brisse S, De Graaf-Miltenburg LA, Troelstra A, Fleer A, et al. Lancet. 2001;357:1674–5.PubMedCrossRefGoogle Scholar
  95. 95.
    Witte W, Cuny C. Future Microbiol. 2011;6:925–31.PubMedCrossRefGoogle Scholar
  96. 96.
    Wulf MW, Verduin CM, Van Nes A, Huijsdens X, Voss A. Eur J Clin Microbiol Infect Dis 2011.Google Scholar
  97. 97.
    Zadoks RN, Watts JL. Vet Microbiol. 2009;134:20–8.PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  1. 1.Department of Veterinary MedicineUniversity of CambridgeCambridgeUK
  2. 2.Moredun Research Institute, Bush LoanPenicuikUK
  3. 3.University of Edinburgh Royal (Dick) School of Veterinary Studies, Easter Bush Veterinary CentreRoslinUK

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