Genotyping of Staphylococcus aureus isolates from diseased poultry

Veterinary Microbiology

Volumn 162, Issue 2-4, 2013, Pages 806-812

  Monecke, Stefan ^a,b   Ruppelt, Antje ^a   Wendlandt, Sarah ^c   Schwarz, Stefan ^c   Slickers, Peter ^b   Ehricht, Ralf ^b   Jäckel, Sonia Cortez de ^d  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b Alere Technologies GmbH   (Germany)

^c FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

^d Poultry Clinics and Laboratory Dr Pöppel   (Germany)

Author keywords

CC398; Dru typing; Microarray analysis; Minimum inhibitory concentrations; MRSA; MSSA; Spa typing; Staphylococcus aureus

Indexed keywords

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIUM ISOLATE; BIRD DISEASE; CHICKEN; DNA MICROARRAY; GENOTYPE; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; NONHUMAN; PHENOTYPE; TURKEY (BIRD);

ANIMALS; ANTI-BACTERIAL AGENTS; ANTIGENS, BACTERIAL; CHICKENS; GENOTYPE; MEAT; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIAL SENSITIVITY TESTS; POULTRY DISEASES; STAPHYLOCOCCAL INFECTIONS; TURKEYS;

GALLUS GALLUS; LONCHOCARPUS GLAUCIFOLIUS; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS AUREUS;

EID: 84872487435     PISSN: 03781135     EISSN: 18732542     Source Type: Journal    
DOI: 10.1016/j.vetmic.2012.10.018     Document Type: Article

References (44)

1. Battisti A., Franco A., Merialdi G., Hasman H., Iurescia M., Lorenzetti R., Feltrin F., Zini M., Aarestrup F.M. Heterogeneity among methicillin-resistant Staphylococcus aureus from Italian pig finishing holdings. Vet. Microbiol. 2010, 142:361-366.
2. Clinical and Laboratory Standards Institute Performance Standards for Antimicrobial Disk and Dilution Susceptibility Test for Bacteria Isolated from Animals; Approved Standard 2008, Clinical and Laboratory Standards Institute, Wayne, PA, CLSI Document M31-A3. third ed.
3. Clinical and Laboratory Standards Institute Performance Standards for Antimicrobial Susceptibility Testing - Twentieth Informational Supplement 2011, Clinical and Laboratory Standards Institute, Wayne, PA, CLSI Document M100-S21.
4. Cui S., Li J., Hu C., Jin S., Li F., Guo Y., Ran L., Ma Y. Isolation and characterization of methicillin-resistant Staphylococcus aureus from swine and workers in China. J. Antimicrob. Chemother. 2009, 64:680-683.
5. De Neeling A.J., Van Den Broek M.J., Spalburg E.C., van Santen-Verheuvel M.G., Dam-Deisz W.D., Boshuizen H.C., Van De Giessen A.W., Van Duijkeren E., Huijsdens X.W. High prevalence of methicillin reistant Staphylococcus aureus in pigs. Vet. Microbiol. 2007, 122:366-372.
6. Deurenberg R.H., Nulens E., Valvatne H., Sebastian S., Driessen C., Craeghs J., de Brauwer E., Heising B., Kraat Y.J., Riebe J., Stals F.S., Trienekens T.A., Scheres J., Friedrich A.W., van Tiel F.H., Beisser P.S., Stobberingh E.E. Cross-border dissemination of methicillin-resistant Staphylococcus aureus, Euregio Meuse-Rhine region. Emerg. Infect. Dis. 2009, 15:727-734.
7. Du J., Chen C., Ding B., Tu J., Qin Z., Parsons C., Salgado C., Cai Q., Song Y., Bao Q., Zhang L., Pan J., Wang L., Yu F. Molecular characterization and antimicrobial susceptibility of nasal Staphylococcus aureus isolates from a Chinese medical college campus. PLoS ONE 2011, 6:e27328.
8. Enright M.C., Day N.P.J., Davies C.E., Peacock S.J., Spratt B.G. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J. Clin. Microbiol. 2000, 38:1008-1015.
9. Feßler A., Scott C., Kadlec K., Ehricht R., Monecke S., Schwarz S. Characterization of methicllin-resistant Staphylococcus aureus ST398 from cases of bovine mastitis. J. Antimicrob. Chemother. 2010, 65:619-625.
10. Feßler A.T., Kadlec K., Hassel M., Hauschild T., Eidam C., Ehricht R., Monecke S., Schwarz S. Characterization of methicillin-resistant Staphylococcus aureus isolates from food and food products of poultry origin in Germany. Appl. Environ. Microbiol. 2011, 77:7151-7157.
11. Goering R.V., Morrison D., Al-Doori Z., Edwards G.F., Gemmell C.G. Usefulness of mec-associated direct repeat unit (dru) typing in the epidemiological analysis of highly clonal methicillin-resistant Staphylococcus aureus in Scotland. Clin. Microbiol. Infect. 2008, 14:964-969.
12. Guardabassi L., O'Donoghue M., Moodley A., Ho J., Boost M. Novel lineage of methicillin-resistant Staphylococcus aureus, Hong Kong. Emerg. Infect. Dis. 2009, 15:1998-2000.
13. 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.
14. Hauschild T., Feßler A.T., Kadlec K., Billerbeck C., Schwarz S. Detection of the novel vga(E) gene in methicillin-resistant Staphylococcus aureus CC398 isolates from cattle and poultry. J. Antimicrob. Chemother. 2012, 67:503-504.
15. Huijsdens X.W., Van Dijke B.J., Spalburg E., Van Santen-Verheuvel M.G., Heck M.E., Pluister G.N., Voss A., Wannet W.J., de Neeling A.J. Community-acquired MRSA and pig-farming. Ann. Clin. Microbiol. Antimircob. 2006, 5:26.
16. Ip M., Yung R.W.H., Ng T.K., Luk W.K., Tse C., Hung P., Enright M., Lyon D.J. Contemporary methicillin-resistant Staphylococcus aureus clones in Hong Kong. J. Clin. Microbiol. 2005, 43:5069-5073.
17. Kadlec K., Ehricht R., Monecke S., Steinacker U., Kaspar H., Mankertz J., Schwarz S. Diversity of antimicrobial resistance pheno- and genotypes of methicillin-resistant Staphylococcus aureus ST398 from diseased swine. J. Antimicrob. Chemother. 2009, 64:1156-1164.
18. Krziwanek K., Metz-Gercek S., Mittermayer H. Methicillin-resistant Staphylococcus aureus ST398 from human patients, upper Austria. Emerg. Infect. Dis. 2009, 15:766-769.
19. Kwon N.H., Park K.T., Jung W.K., Youn H.Y., Kim S.H., Bae W., Lim J.Y., Kim J.Y., Kim J.M., Hong S.K., Park Y.H. Characteristics of methicillin resistant Staphylococcus aureus isolated from chicken meat and hospitalized dogs in Korea and their epidemiological relatedness. Vet. Microbiol. 2006, 117:304-312.
20. Lowder B.V., Guinane C.M., Ben Zakour N.L., Weinert L.A., Conway-Morris A., Cartwright R.A., Simpson A.J., Rambaut A., Nübel U., Fitzgerald J.R. Recent human-to-poultry host jump, adaptation, and pandemic spread of Staphylococcus aureus. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:19545-19550.
21. Lozano C., Lopez M., Gomez-Sanz E., Ruiz-Larrea F., Torres C., Zarazaga M. Detection of methicillin-resistant Staphylococcus aureus ST398 in food samples of animal origin in Spain. J. Antimicrob. Chemother. 2009, 64:1325-1326.
22. Monecke S., Kuhnert P., Hotzel H., Slickers P., Ehricht R. Microarray-based study on virulence-associated genes and resistance determinants of Staphylococcus aureus isolates from cattle. Vet. Microbiol. 2007, 125:128-140.
23. Monecke S., Luedicke C., Slickers P., Ehricht R. Molecular epidemiology of Staphylococcus aureus in asymptomatic carriers. Eur. J. Clin. Microbiol. Infect. Dis. 2009, 28:1159-1165.
24. Monecke S., Coombs G., Shore A.C., Coleman D.C., Akpaka P., Borg M., Chow H., Ip M., Jatzwauk L., Jonas D., Kadlec K., Kearns A., Laurent F., O'Brien F.G., Pearson J., Ruppelt A., Schwarz S., Scicluna E., Slickers P., Tan H.-L., Weber S., Ehricht R. A field guide to pandemic, epidemic and sporadic clones of methicillin-resistant Staphylococcus aureus. PLoS ONE 2011, e17936.
25. Monecke S., Engelmann I., Archambault M., Coleman D.C., Coombs G.W., Cortez de Jackel S., Pelletier-Jacques G., Schwarz S., Shore A.C., Slickers P., Ehricht R. Distribution of SCCmec-associated phenol-soluble modulin in staphylococci. Mol. Cell. Probes 2012, 26:99-103.
26. Monecke S., Skakni L., Hasan R., Ruppelt A., Ghazal S.S., Hakawi A., Slickers P., Ehricht R. Characterisation of MRSA strains isolated from patients in a hospital in Riyadh, Kingdom of Saudi Arabia. BMC Microbiol. 2012, 12:146.
27. Neela V., Mohd Zaful A., Mariana N.S., van Belkum A., Liew Y.K., Rad E.G. Prevalence of ST9 methicillin-resistant Staphylococcus aureus among pigs and pig handlers in Malaysia. J. Clin. Microbiol. 2009, 47:4138-4140.
28. Nemati M., Hermans K., Lippinska U., Denis O., Deplano A., Struelens M., Devriese L.A., Pasmans F., Haesebrouck F. Antimicrobial resistance of old and recent Staphylococcus aureus isolates from poultry: first detection of livestock-associated methicillin-resistant strain ST398. Antimicrob. Agents Chemother. 2008, 52:3817-3819.
29. Nienhoff U., Kadlec K., Chaberny I.F., Verspohl J., Gerlach G.F., Schwarz S., Simon D., Nolte I. Transmission of methicillin-resistant Staphylococcus aureus strains between humans and dogs: two case reports. J. Antimicrob. Chemother. 2009, 64:640-662.
30. Nimmo G.R., Coombs G.W. Community-associated methicillin-resistant Staphylococcus aureus (MRSA) in Australia. Int. J. Antimicrob. Agents 2008, 31:401-410.
31. Pan A., Battisti A., Zoncada A., Bernieri F., Boldini M., Franco A., Giorgi M., Iurescia M., Lorenzotti S., Martinotti M., Monaci M., Pantosti A. Community-acquired methicillin-resistant Staphylococcus aureus ST398 infection, Italy. Emerg. Infect. Dis. 2009, 15:845-847.
32. Potel C., Ãlvarez-Fernandez M., Constenla L., Ãlvarez P., Perez S. First human isolates of methicillin-resistant Staphylococcus aureus sequence type 398 in Spain. Eur. J. Clin. Microbiol. Infect. Dis. 2010, 29:351-352.
33. Price L.B., Stegger M., Hasman H., Aziz M., Larsen J., Andersen P.S., Pearson T., Waters A.E., Foster J., Schupp J., Gillec J., Driebe E., Liu C.M., Laurent F., Springer B., Zdovc I., Battisti A., Franco A., Zmudzki J., Schwarz S., Butaye P., Jouy E., Pomba C., Porreo M.C., Smith T.C., Robinson D.A., Weese J.S., Arriola C.O., Yu F., Ruimy R., Keim P., Skov R., Aarestrup F.M. Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock. mBio 2012, 3:e00305-e00311.
34. Schijffelen M.J., Boel C.H., van Strijp J.A., Fluit A.C. Whole genome analysis of a livestock-associated methicillin-resistant Staphylococcus aureus ST398 isolate from a case of human endocarditis. BMC Genomics 2010, 11:376.
35. Schwarz S., Silley P., Simjee S., Woodford N., van Duijkeren E., Johnson A.P., Gaastra W. Assessing the antimicrobial susceptibility of bacteria obtained from animals. Vet. Microbiol. 2010, 141:1-4.
36. Shittu A., Nübel U., Udo E., Lin J., Gaogakwe S. Characterisation of methicillin-resistant Staphylococcus aureus isolates from hospitals in KwaZulu-Natal province, Republic of South Africa. J. Med. Microibiol. 2009, 58:1219-1226.
37. Soavi L., Stellini R., Signorini L., Antonini B., Pedroni P., Zanetti L., Milanesi B., Pantosti A., Matteelli A., Pan A., Carosi G. Methicillin-resistant Staphylococcus aureus ST398, Italy. Emerg. Infect. Dis. 2010, 16:346-348.
38. Van Duijkeren E., Ikawaty R., Broekhuizen-Stins M.J., Jansen M.D., Spalburg E.C., de Neeling A.J., Allaart J.G., van Nes A., Wagenaar J.A., Fluit A.C. Transmission of methicillin-resistant Staphylococcus aureus strains between different kinds of pig farms. Vet. Microbiol. 2008, 126:383-389.
39. Van Loo I., Huijsdens X., Tiermersma E., De Neeling A., Van de Sande-Bruinsma N., Beaujean D., Voss A., Klytmans J. Emergence of methisillin-resistant Staphylococcus aureus of animal origin in humans. Emerg. Infect. Dis. 2007, 13:1834-1839.
40. 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.
41. Vestergaard M., Cavaco L.M., Sirichote P., Unahalekhaka A., Dangsakul W., Svendsen C.A., Aarestrup F.M., Hendriksen R.S. SCCmec type IX element in methicillin resistant Staphylococcus aureus spa type t337 (CC9) isolated from pigs and pork in Thailand. Front. Microbiol. 2012, 3:103.
42. Wagenaar J.A., Yue H., Pritchard J., Broekhuizen-Stins M., Huijsdens X., Mevius D.J., Bosch T., van Duijkeren E. Unexpected sequence types in livestock associated methicillin-resistant Staphylococcus aureus (MRSA): MRSA ST9 and a single locus variant of ST9 in pig farming in China. Vet. Microbiol. 2009, 139:405-409.
43. Walther B., Monecke S., Ruscher C., Friedrich A.W., Ehricht R., Slickers P., Soba A., Wleklinski C.G., Wieler L.H., Lubke-Becker A. Comparative molecular analysis substantiates a zoonotic potential of equine methicillin-resistant Staphylococcus aureus (MRSA). J. Clin. Microbiol. 2009, 47:704-710.
44. Wulf M., Van Nes A., Eikelenboom-Boskamp A., De Vries J., Melchers W., Klaassen C., Voss A. Methicillin-resistant Staphylococcus aureus in veterinary doctors and students, The Netherlands. Emerg. Infect. Dis. 2006, 12:1939-1941.