Diversity and antimicrobial susceptibility profiling of staphylococci isolated from bovine mastitis cases and close human contacts

Journal of Dairy Science

Volumn 98, Issue 9, 2015, Pages 6256-6269

  Schmidt, T ^a,b   Kock, M M ^a,c   Ehlers, M M ^a,c  

^a UNIVERSITY OF PRETORIA   (South Africa)

^b KwaZulu Natal Department of Agriculture   (South Africa)

^c NATIONAL HEALTH LABORATORY SERVICE   (South Africa)

Author keywords

Antimicrobial resistance; Bovine mastitis; Close human contact; Staphylococcus spp

Indexed keywords

ANIMALIA; BOVINAE; STAPHYLOCOCCUS;

BACTERIAL PROTEIN; MECA PROTEIN, STAPHYLOCOCCUS AUREUS; PENICILLIN BINDING PROTEIN;

ANIMAL; BACTERIAL GENE; BIODIVERSITY; BOVINE; CLASSIFICATION; DRUG EFFECTS; FEMALE; GENETICS; HUMAN; ISOLATION AND PURIFICATION; MASS SPECTROMETRY; MASTITIS, BOVINE; MICROBIOLOGY; MILK; MULTIDRUG RESISTANCE; SOUTH AFRICA; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS; VETERINARY;

ANIMALS; BACTERIAL PROTEINS; BIODIVERSITY; CATTLE; DRUG RESISTANCE, MULTIPLE, BACTERIAL; FEMALE; GENES, BACTERIAL; HUMANS; MASTITIS, BOVINE; MILK; PENICILLIN-BINDING PROTEINS; SOUTH AFRICA; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS;

EID: 84939189795     PISSN: 00220302     EISSN: 15253198     Source Type: Journal    
DOI: 10.3168/jds.2015-9715     Document Type: Article

References (66)

1. Akineden Ö., Annemüller C., Hassan A., Lämmler C., Wolter W., Zschöck M. Toxin genes and other characteristics of Staphylococcus aureus isolates from milk of cows with mastitis. Clin. Diagn. Lab. Immunol. 2001, 8:959-964.
2. Ateba C.N., Mbewe M., Moneoang M.S., Bezuidenhout C.C. Antibiotic-resistant Staphylococcus aureus isolated from milk in the Mafikeng area, North West Province, South Africa. S. Afr. J. Sci. 2010, 106. http://dx.doi.org/10.4102/sajs.v106i11/12.243.
3. 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.
4. Barreiro J.R., Ferreira C.R., Sanvido G.B., Kostrzewa M., Maier T., Wegemann B., Böttcher V., Eberlin M.N., dos Santos M.V. Short communication: Identification of subclinical cow mastitis pathogens in milk by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. J. Dairy Sci. 2010, 93:5661-5667.
5. Capurro A., Artursson K., Persson Waller K., Bengtsson B., Ericsson-Unnerstad H., Aspán A. Comparison of a commercialized phenotyping system, antimicrobial susceptibility testing, and tuf gene sequenced-based genotyping for species-level identification of coagulase-negative staphylococci isolated from cases of bovine mastitis. Vet. Microbiol. 2009, 134:327-333.
6. Chambers H.F., DeLeo F.R. Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat. Rev. Microbiol. 2009, 7:629-641.
7. Chiang Y.-C., Lu H.-C., Li S.-C., Chang Y.-H., Chen H.-Y., Lin C.-W., Tsen H.-Y. Development of PCR primers and a DNA macroarray for the simultaneous detection of major Staphylococcus species using groESL gene. Foodborne Pathog. Dis. 2012, 9:249-257.
8. Clark N.C., Cooksey R.C., Hill B.C., Swenson J.M., Tenover F.C. Characterization of glycopeptide-resistant enterococci from U.S. hospitals. Antimicrob. Agents Chemother. 1993, 37:2311-2317.
9. CLSI (Clinical Laboratory Standards Institute). 2008. Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated From Animals-Third Edition: Vol. 28, No. 8. Approved Standard M31-A3. Clinical Laboratory Standards Institute, Wayne, PA.
10. CLSI (Clinical Laboratory Standards Institute). 2014. Performance Standards for Antimicrobial Susceptibility Testing: Twenty-fourth International Supplement. CLSI document M100-S24: Vol. 34, No. 1. Clinical Laboratory Standards Institute, Wayne, PA.
11. El Behiry A., Zahran R.M., Marzouk E., Al-Dabib M. Phenotypical and mass spectral assessment methods for identification of some contagious mastitis pathogens. Am. J. Microbiol. 2013, 4:32-41.
12. EUCAST (European Committee on Antimicrobial Susceptibility Testing). 2014. Breakpoint tables for the interpretation of MICs and zone diameters. Version 4.0, 2014. http://http://www.eucast.org.
13. Fiebelkorn K.R., Crawford S.A., McElmeel M.L., Jorgensen J.H. Practical disk diffusion method for detection of inducible clindamycin resistance in Staphylococcus aureus and coagulase-negative staphylococci. J. Clin. Microbiol. 2003, 41:4740-4744.
14. Fitzgerald J.R. Livestock-associated Staphylococcus aureus: Origin, evolution and public health threat. Trends Microbiol. 2012, 20:192-198. http://dx.doi.org/10.1016/j.tim.2012.01.006.
15. Fluit A.C., Visser M.R., Schmitz F.-J. Molecular detection of antimicrobial resistance. Clin. Microbiol. Rev. 2001, 14:836-871.
16. Frey Y., Rodriguez J.P., Thomann A., Schwendener S., Perreten V. Genetic characterization of antimicrobial resistance in coagulase-negative staphylococci from bovine mastitis milk. J. Dairy Sci. 2013, 96:2247-2257.
17. García-Álvarez L., Holden M., Lindsay H., Webb C., Brown D., Curran M., Walpole E., Brooks K., Pickard D., Teale C., Parkhill J., Bentley S., Edwards G., Girvan E., Kearns A., Pichon B., Hill R., Larsen A., Skov R., Peacock S., Maskell D., Holmes M. Methicillin-resistant Staphylococcus aureus with a novel mecA homologue in human and bovine populations in the UK and Denmark: A descriptive study. Lancet Infect. Dis. 2011, 11:595-603.
18. Gentilini E., Denamiel G., Llorente P., Godaly S., Rebuelto M., DeGregorio O. Antimicrobial susceptibility of Staphylococcus aureus isolated from bovine mastitis in Argentina. J. Dairy Sci. 2000, 83:1224-1227.
19. Graveland H., Duim B., van Duijkeren E., Heederik D., Wagenaar J. Livestock-associated methicillin-resistant Staphylococcus aureus in animals and humans. Int. J. Med. Microbiol. 2011, 301:630-634.
20. Heikens E., Fleer A., Paauw A., Florijn A., Fluit A. Comparison of genotypic and phenotypic methods for species-level identification of clinical isolates of coagulase-negative staphylococci. J. Clin. Microbiol. 2005, 43:2286-2290.
21. Hirotaki S., Sasaki T., Kuwahara-Arai K., Hiramatsu K. Rapid and accurate identification of human-associated staphylococci by use of multiplex PCR. J. Clin. Microbiol. 2011, 49:3627-3631.
22. Holmes M.A., Zadoks R.N. Methicillin resistant S. aureus in human and bovine mastitis. J. Mammary Gland Biol. Neoplasia 2011, 16:373-382.
23. IVS. 2015. Index of Veterinary Specialities. Vol 53. Hirt and Carter, Durba, South Africa.
24. Juhász-Kaszanyitzky É., Jánosi S., Somogyi P., Dán Á., van der Graaf-van Bloois L., van Duijkeren E., Wagenaar J. MRSA transmission between cows and humans. Emerg. Infect. Dis. 2007, 13:630-632.
25. Kim H.B., Jang H.-C., Nam H.J., Lee Y.S., Kim B.S., Park W.B., Lee K.D., Choi Y.J., Park S.W., Oh M.D., Kim E.-C., Choe K.W. In vitro activities of 28 antimicrobial agents against Staphylococcus aureus isolates from tertiary-care hospitals in Korea: A nationwide survey. Antimicrob. Agents Chemother. 2004, 48:1124-1127.
26. Kluytmans J., Struelans M. Methicillin-resistant Staphylococcus aureus in the hospital. BMJ 2009, 338:b364.
27. Lindsay J.A., Holden M.T.G. Understanding the rise of the superbug: Investigation of the evolution and genomic variation of Staphylococcus aureus. Funct. Integr. Genomics 2006, 6:186-201.
28. Lowy F. Staphylococcal infections. Harrison's Principles of Internal Medicine 2013, 159-170. McGraw-Hill, New York, NY. 18th. D.L. Longo, A.S. Fauci, D.L. Kasper, S.>.L. Hauser, J.J. Jameson, J. Loscalzo (Eds.).
29. LPSN. 2015. List of Prokaryotic Names with Standing in Nomenclature. Accessed Apr. 8, 2015. http://http://www.bacterio.net/staphylococcus.html.
30. McClure J.-A., Conly J.M., Lau V., Elsayed S., Louie T., Hutchins W., Zhang K. Novel Multiplex PCR assay for detection of staphylococcal virulence marker Panton-Valentine leukocidin genes and simultaneous discrimination of methicillin-susceptible from -resistant staphylococci. J. Clin. Microbiol. 2006, 44:1141-1144.
31. Morley P.S., Apley M.D., Besser T.E., Burney D.P., Fedorka-Cray P.J., Papich M.G., Traub-Dargatz J.L., Weese J.S. Antimicrobial drug use in veterinary medicine. J. Vet. Intern. Med. 2005, 19:617-629.
32. Otto M. Coagulase-negative staphylococci as reservoirs of genes facilitating MRSA infection. BioEssays 2013, 35:4-11.
33. Pantosti A., Sanchini A., Monaco M. Mechanisms of antibiotic resistance in Staphylococcus aureus. Future Microbiol. 2007, 2:323-334.
34. Park J.-Y., Fox L.K., Seo K.S., McGuire M.A., Park Y.H., Rurangirwa F.R., Sischo W.M., Bohach G.A. Comparison of phenotypic and genotypic methods for the species identification of coagulase-negative staphylococcal isolates from bovine intramammary infections. Vet. Microbiol. 2011, 147:142-148.
35. Persson Waller K., Aspán A., Nyman A., Persson Y., Andersson U.G. CNS species and antimicrobial resistance in clinical and subclinical bovine mastitis. Vet. Microbiol. 2011, 152:112-116.
36. Petzer, I.-M., J. Karzis, T. J. van der Schans, J. C. Watermeyer, and M. Smither. 2007. Antibiotic efficacy against staphylococcal udder pathogens in dairy cows in South Africa from 2000 to 2006. Pages 33-49. Livestock Health and Production Group of the South African Veterinary Association Congress. Vetlink, Pretoria, South Africa.
37. Petzer I.-M., Karzis J., Watermeyer J., van der Schans T.J., van Reenen R. Trends in udder health and emerging mastitogenic pathogens in South African dairy herds. J. S. Afr. Vet. Assoc. 2009, 80:17-22.
38. Piessens V., van Coillie E., Verbist B., Supre K., Braem G., van Nuffel A., de Vuyst L. Distribution of coagulase-negative Staphylococcus species from milk and environment of dairy cows differs between herds. J. Dairy Sci. 2011, 94:2933-2944.
39. Pyörälä S., Simojoki H., Taponen S. News about mastitis-causing staphylococci 2011, European Buiatrics Forum, Marseille, France.
40. Quinn P.J., Carter M.E., Markey B., Carter G.R. Staphylococcus species. Clinical Veterinary Microbiology 1999, Mosby, Madrid, Spain, Pages 118-126.
41. Sampimon O.C., Lam T., Mevius D., Schukken Y., Zadoks R. Antimicrobial susceptibility of coagulase-negative staphylococci isolated from bovine milk samples. Vet. Microbiol. 2011, 150:173-179.
42. Sasaki T., Tsubakishita S., Tanaka Y., Sakusabe A., Ohtsuka M., Hirotaki S., Kawakami T., Fukata T., Hiramatsu K. Multiplex-PCR method for species identification of coagulase-positive staphylococci. J. Clin. Microbiol. 2010, 48:765-769.
43. Sawant A.A., Gillespie B.E., Oliver S. Antimicrobial susceptibility of coagulase-negative Staphylococcus species isolated from bovine milk. Vet. Microbiol. 2009, 134:73-81.
44. Schmidt T. In vitro antimicrobial susceptibility of Staphylococcus aureus strains from dairy herds in KwaZulu-Natal. J. S. Afr. Vet. Assoc. 2011, 82:76-79.
45. Schwarz S., Silley P., Simjee S., Woodford N., van Duijkeren E., Johnson A., Gaastra W. Editorial: Assessing the antimicrobial susceptibility of bacteria obtained from animals. J. Antimicrob. Chemother. 2010, 65:601-604.
46. Shittu A.O., Lin J. Antimicrobial susceptibility patterns and characterization of clinical isolates of Staphylococcus aureus in KwaZulu-Natal province, South Africa. BMC Infect. Dis. 2006, 6:125.
47. Shome B.R., Das Mitra S., Bhuvana M., Krithiga N., Velu D., Shome R., Isloor S., Barbuddhe S.B., Rahman H. Multiplex PCR assay for species identification of bovine mastitis pathogens. J. Appl. Microbiol. 2011, 111:1349-1356.
48. LGA251. Clin. Microbiol. Infect. 2012, 18:395-400.
49. Strommenger B., Kettlitz C., Werner G., Witte W. Multiplex PCR assay for simultaneous detection of nine clinically relevant antibiotic resistance genes in Staphylococcusaureus. J. Clin. Microbiol. 2003, 41:4089-4094.
50. Supré K., De Vliegher S., Cleenwerck I., Engelbeen K., Van Trappen S., Piepers S., Sampimon O.S., Zadoks R.N., De Vos P., Haesebrouck F. Staphylococcus devriesei sp. nov., isolated from teat apices and milk of dairy cows. Int. J. Syst. Evol. Microbiol. 2010, 60:2739-2744.
51. Supré K., Haesebrouck F., Zadoks R.N., Vaneechoutte M., Piepers S., De Vliegher S. Some coagulase-negative Staphylococcus species affect udder health more than others. J. Dairy Sci. 2011, 94:2329-2340.
52. Taponen S. Bovine mastitis caused by coagulase-negative staphylococci. Doctoral Diss. Univ 2008, Helsinki, Helsinki, Finland.
53. Taponen S., Pyörälä S. Coagulase-negative staphylococci as cause of bovine mastitis - not so different from Staphylococcus aureus?. Vet. Microbiol. 2009, 134:29-36.
54. Taponen S., Supré K., Piessens V., van Coillie E., De Vliegher S., Koort J.M.K. Staphylococcus agnetis sp. nov., a coagulase-variable species from bovine subclinical and mild clinical mastitis. Int. J. Syst. Evol. Microbiol. 2012, 62:61-65.
55. Tenhagen B.A., Koster G., Wallmann J., Heuwieser W. Prevalence of mastitis pathogens and their resistance against antimicrobial agents in dairy cows in Brandenburg, Germany. J. Dairy Sci. 2006, 89:2542-2551.
56. Thorberg B.M., Danielsson-Tham M.L., Emanuelson U., Persson Waller K. Bovine subclinical mastitis caused by different types of coagulase-negative staphylococci. J. Dairy Sci. 2009, 92:4962-4970.
57. Thorberg B.M., Kühn I., Aarestrup F., Brändström B., Jonsson P., Danielsson-Tham M.-L. Pheno- and genotyping of Staphylococcus epidermidis isolated from bovine milk and human skin. Vet. Microbiol. 2006, 115:163-172.
58. Unnerstad H.E., Bengtsson B., Horn af Rantzien M., Börjesson S. Methicillin-resistant Staphylococcus aureus containing mecC in Swedish dairy cows. Acta Vet. Scand. 2013, 55:6. http://dx.doi.org/10.1186/1751-0147-55-6.
59. Vanderhaeghen W., Cerpentier T., Adriaensen C., Vicca J., Hermans K., Butaye P. Methicillin-resistant Staphylococcus aureus (MRSA) ST398 associated with clinical and subclinical mastitis in Belgian cows. Vet. Microbiol. 2010, 144:166-171.
60. Vanderhaeghen W., Piepers S., Leroy F., van Coillie E., Haesebrouck F., De Vliegher S. Identification, typing, ecology and epidemiology of coagulase negative staphylococci associated with ruminants. Vet. J. 2015, 203:44-51. http://dx.doi.org/10.1016/j.tvjl.2014.11.001.
61. Vesterholm-Nielsen M., Larsen M., Olsen J., Aarestrup F. Occurrence of the blaZ gene in penicillin resistant Staphylococcus aureus isolated from bovine mastitis in Denmark. Acta Vet. Scand. 1999, 40:279-286.
62. Vitali L.A., Petrelli D., Lamikanra A., Prenna M., Akinkunmi E.O. Diversity of antibiotic resistance genes and staphylococcal cassette chromosome mec elements in faecal isolates of coagulase-negative staphylococci from Nigeria. BMC Microbiol. 2014, 14:106.
63. Wieser A., Schneider L., Jung J., Schubert S. MALDI-TOF MS in microbiological diagnostics-Identification of microorganisms and beyond (mini review). Appl. Microbiol. Biotechnol. 2012, 93:965-974.
64. Zadoks R.N., van Leeuwen W.B., Kreft D., Fox L.K., Barkema H.W., Schukken Y.H., van Belkum A. Comparison of Staphylococcus aureus from bovine and human skin, milking equipment, and bovine milk by phage typing, pulsed-field gel electrophoresis, and binary typing. J. Clin. Microbiol. 2002, 40:3894-3902.
65. Zadoks R.N., Watts J.L. Species identification of coagulase-negative staphylococci: Genotyping is superior to phenotyping. Vet. Microbiol. 2009, 134:20-28.
66. Zriouil S.B., Bekkali M., Zerouali K. Epidemiology of Staphylococcus aureus infections and nasal carriage at the Ibn Rochd University hospital center, Casablanca, Morocco. Braz. J. Infect. Dis. 2012, 16:279-283.