Methicillin-resistant Staphylococcus aureus from infections in horses in Germany are frequent colonizers of veterinarians but rare among MRSA from infections in humans

One Health

Volumn 2, Issue , 2016, Pages 11-17

  Cuny, Christiane ^a   Abdelbary, Mohamed M H ^a,d   Köck, Robin ^b,e   Layer, Franziska ^a   Scheidemann, Wolfgang ^c   Werner, Guido ^a   Witte, Wolfgang ^a  

^a ROBERT KOCH INSTITUTE   (Germany)

^b UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^c Tierärztliche Klinik für Pferde   (Germany)

^d LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^e KLINIKUM OLDENBURG   (Germany)

Author keywords

Equine clinic associated MRSA; Host specificity; MRSA; Zoonotic transmission

Indexed keywords

CIPROFLOXACIN; CLINDAMYCIN; COTRIMOXAZOLE; DAPTOMYCIN; ERYTHROMYCIN; FOSFOMYCIN; FUSIDIC ACID; GENTAMICIN; LINEZOLID; MOXIFLOXACIN; OXACILLIN; PENICILLIN DERIVATIVE; POLYPEPTIDE ANTIBIOTIC AGENT; PSEUDOMONIC ACID; RIFAMPICIN; TEICOPLANIN; TETRACYCLINE; TIGECYCLINE; VANCOMYCIN;

ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL COUNT; BACTERIAL STRAIN; BACTERIAL TRANSMISSION; BACTERIUM CARRIER; BACTERIUM ISOLATE; CLADISTICS; CONTROLLED STUDY; GERMANY; HEALTH CARE PERSONNEL; HORSE DISEASE; HUMAN; MAJOR CLINICAL STUDY; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS INFECTION; MOLECULAR CLONING; MOLECULAR TYPING; NONHUMAN; OCCUPATIONAL EXPOSURE; PROSPECTIVE STUDY; VETERINARIAN; VETERINARY CLINIC;

EID: 84952332461     PISSN: None     EISSN: 23527714     Source Type: Journal    
DOI: 10.1016/j.onehlt.2015.11.004     Document Type: Article

References (56)

1. De Lencastre H., Oliveira D., Tomasz A. Antibiotic resistant Staphylococcus aureus: a paradigm of adaptive power. Curr. Opin. Microbiol. 2007, 10:428-445.
2. Palavecino E.L. Clinical, epidemiologic, and laboratory aspects of methicillin-resistant Staphylococcus aureus infections. Methods Mol. Biol. 2014, 1085:1-24.
3. Deurenberg R.H., Vink C., Kalenic S., Friedrich A.W., Bruggeman C.A., Stobberingh E.E. The molecular evolution of methicillin-resistant Staphylococcus aureus. Clin. Microbiol. Infect. 2007, 13:222-235.
4. Enright M.C., Robinson D.A., Randle G., Feil E.J., Grundmann H., Spratt B.G. The evolutionary history of methicillin-resistant Staphylococcus aureus (MRSA). Proc. Natl. Acad. Sci. U. S. A. 2002, 99:7687-7692.
5. Witte W., Cuny C., Klare I., Nübel U., Strommenger B., Werner G. Emergence and spread of antibiotic-resistant Gram-positive bacterial pathogens. Int. J. Med. Microbiol. 2008, 298:365-377.
6. Mediavilla J.R., Chen L., Mathema B., Kreiswirth B.N. Global epidemiology of community-associated methicillin resistant Staphylococcus aureus (CA-MRSA). Curr. Opin. Microbiol. 2012, 15:588-595.
7. Hartmann F.A., Trostle S.S., Klohnen A.A. Isolation of methicillin-resistant Staphylococcus aureus from a postoperative wound infection in a horse. J. Am. Vet. Med. Assoc. 1997, 1:590-592.
8. Cuny C., Friedrich A., Kozytska S., Layer F., Nübel U., Ohlsen K., Strommenger B., Walther B., Wieler L., Witte W. Emergence of methicillin-resistant Staphylococcus aureus (MRSA) in different animal species. Int. J. Med. Microbiol. 2010, 300:109-117.
9. Graveland H., Duim B., van Duijkeren E., Heederik D., Wagenaar J.A. Livestock-associated methicillin-resistant Staphylococcus aureus in animals and humans. Int. J. Med. Microbiol. 2011, 301:630-634.
10. Cuny C., Köck R., Witte W. Livestock associated MRSA (LA-MRSA) and its relevance for humans in Germany. Int. J. Med. Microbiol. 2013, 303:331-337.
11. Köck R., Schaumburg F., Mellmann A., Köksal M., Jurke A., Becker K., Friedrich A.W. Livestock-associated methicillin-resistant Staphylococcus aureus (MRSA) as causes of human infection and colonization in Germany. PLoS One 2013, 8.
12. Pantosti A. Methicillin-resistant Staphylococcus aureus associated with animals and its relevance to human health. Front. Microbiol. 2012, 3:127.
13. Lin Y., Barker E., Kislow J., Kaldhone P., Stemper M.E., Pantrangi M., Moore F.M., Hall M., Fritsche T.R. Evidence of multiple virulence subtypes in nosocomial and community-associated MRSA genotypes in companion animals from the upper Midwestern and Northeastern United States. Clin. Med. Res. 2011, 9:7-16.
14. Walther B., Monecke S., Ruscher C., Friedrich A.W., Ehricht R., Slickers P., Soba A., Wleklinski C.G., Wieler L.H., Lübke-Becker A. Comparative molecular analysis substantiates zoonotic potential of equine methicillin-resistant Staphylococcus aureus. J. Clin. Microbiol. 2009, 47:704-710.
15. Weese J.S. Methicillin-resistant Staphylococcus aureus: an emerging pathogen in small animals. J. Am. Anim. Hosp. Assoc. 2005, 41:150-157.
16. Harrison E.M., Paterson G.K., Holden M.T., Larsen J., Stegger M., Larsen A.R., Petersen A., Skov R.L., Christensen J.M., Bak Zeuthen A., Heltberg O., Harris S.R., Zadoks R.N., Parkhill J., Peacock S.J., Holmes M.A. A shared population of epidemic methicillin-resistant Staphylococcus aureus 15 circulates in humans and companion animals. MBio 2014, 5. (e00985-13).
17. Loeffler A., Lloyd D.H. Companion animals: a reservoir for methicillin- resistant Staphylococcus aureus in the community?. Epidemiol. Infect. 2010, 138:595-605.
18. Seguin J.C., Walker R.D., Caron J.P., Kloos W.E., George C.G., Hollis R.J., Jones R.N., Pfaller M.A. Methicillin-resistant Staphylococcus aureus outbreak in a veterinary teaching hospital: potential human-to-animal transmission. J. Clin. Microbiol. 1999, 37:1459-1464.
19. Weese J.S. Methicillin-resistant Staphylococcus aureus in horses and horse personnel. Vet. Clin. North Am. Equine Pract. 2004, 20:601-613.
20. Weese J.S., Rousseau J., Willey B.M., Archambault M., McGeer A., Low D.E. Methicillin-resistant Staphylococcus aureus in horses at a veterinary teaching hospital: frequency, characterization, and association with clinical disease. J. Vet. Intern. Med. 2006, 20:182-186.
21. Friedrich A., Walther B., Lübke-Becker A., Wieler L.H. Methicillin resistant Staphylococcus aureus in a modern animal hospital-professional infection management. Prakt. Tierarztl. 2004, 85:742-748.
22. Cuny C., Strommenger B., Witte W., Stanek C. Clusters of infections in horses with MRSA ST1, ST254, and ST398 in a veterinary hospital. Microb. Drug Resist. 2008, 14:307-310.
23. Simor A.E., Ofner-Agostini M., Bryce E., McGeer A., Paton S., Mulvey M.R. Canadian Hospital Epidemiology Committee and Canadian Nosocomial Infection Surveillance Program, Health Canada. Laboratory characterization of methicillin-resistant Staphylococcus aureus in Canadian hospitals: results of 5 years of National Surveillance, 1995-1999. J. Infect. Dis. 2002, 186:652-660.
24. Moodley A., Stegger M., Bagcigil A.F., Baptiste K.E., Loeffler A., Lloyd D.H., Williams N.J., Leonard N., Abbott Y., Skov R., Guardabassi L. Spa typing of methicillin-resistant Staphylococcus aureus isolated from domestic animals and veterinary staff in the UK and Ireland. J. Antimicrob. Chemother. 2006, 58:1118-1123.
25. O'Mahony R., Abbott Y., Leonard F.C., Markey B.K., Quinn P.J., Pollock P.J., Fanning S., Rossney A.S. Methicillin-resistant Staphylococcus aureus (MRSA) isolated from animals and veterinary personnel in Ireland. Vet. Microbiol. 2005, 109:285-296.
26. Weese J.S., Caldwell F., Willey B.M., Kreiswirth B.N., McGeer A., Rousseau J., Low D.E. An outbreak of methicillin-resistant Staphylococcus aureus skin infections resulting from horse to human transmission in a veterinary hospital. Vet. Microbiol. 2006, 114:160-164.
27. Loncaric I., Künzel F., Licka T., Simhofer H., Spergser J., Rosengarten R. Identification and characterization of methicillin-resistant Staphylococcus aureus (MRSA) from Austrian companion animals and horses. Vet. Microbiol. 2014, 168:381-387.
28. Hermans K., Lipinska U., Denis O., Deplano A., Struelens M.J., Nemati M., Pasmans F., Butaye P., Martens A., Deprez P., Haesebrouck F. MRSA clone ST398-SCCmecIV as a cause of infections in an equine clinic. Vlaam. Diergeneeskd. Tijdschr. 2008, 77:429-433.
29. Van den Eede A., Martens A., Lipinska U., Struelens M., Deplano A., Denis O., Haesebrouck F., Gasthuys F., Hermans K. High occurrence of methicillin-resistant Staphylococcus aureus ST398 in equine nasal samples. Vet. Microbiol. 2009, 133:138-144.
30. Vincze S., Stamm I., Kopp P.A., Hermes J., Adlhoch C., Semmler T., Wieler L.H., Lübke-Becker A., Walther B. Alarming proportions of methicillin-resistant Staphylococcus aureus (MRSA) in wound samples from companion animals, Germany 2010-2012. PLoS One 2014, 9.
31. van Duijkeren E., Moleman M., Sloet van Oldruitenborgh-Oosterbaan M.M., Multem J., Troelstra A., Fluit A.C., van Wamel W.J., Houwers D.J., de Neeling A.J., Wagenaar J. Methicillin-resistant Staphylococcus aureus in horses and horse personnel: an investigation of several outbreaks. Vet. Microbiol. 2010, 141:96-102.
32. Sieber S., Gerber V., Jandova V., Rossano A., Evison J.M., Perreten V. Evolution of multidrug-resistant Staphylococcus aureus infections in horses and colonized personnel in an equine clinic between 2005 and 2010. Microb. Drug Resist. 2011, 17:471-478.
33. Van den Eede A., Martens A., Floré K., Denis O., Gasthuys F., Haesebrouck F., Van den Abeele A., Hermans K. MRSA carriage in the equine community: an investigation of horse-caretaker couples. Vet. Microbiol. 2013, 163:313-318.
34. Abdelbary M.M.H., Wittenberg A., Cuny C., Layer F., Kurt K., Wieler L.H., Walther B., Skov R., Larsen J., Hasman H., Fitzgerald J.R., Smith T.C., Wagenaar J.A., Pantosti A., Hallin M., Struelens M.J., Edwards G., Böse R., Nübel U., Witte W. Phylogenetic analysis of Staphylococcus aureus CC398 reveals a sub-lineage epidemiologically associated with infections in horses. PLoS One 2014, 9.
35. Cuny C., Nathaus R., Layer F., Strommenger B., Altmann D., Witte W. Nasal colonization of humans with methicillin-resistant Staphylococcus aureus (MRSA) CC398 with and without exposure to pigs. PLoS One 2009, 4.
36. Cuny C., Layer F., Werner G., Harmsen D., Daniels-Haardt I., Jurke A., Mellmann A., Witte W., Köck R. State-wide surveillance of antibiotic resistance patterns and spa types of Methicillin-resistant Staphylococcus aureus from blood cultures in North -Rhine- Westphalia, 2011-2013. Clin. Microbiol. Infect. 2015, 21:750-757.
37. Cuny C., Layer F., Strommenger B., Witte W. Rare occurrence of methicillin-resistant Staphylococcus aureus CC130 with a novel mecA homologue in humans in Germany. PLoS One 2011, 6.
38. Cuny C., Abdelbary M., Layer F., Werner G., Witte W. Prevalence of the immune evasion gene cluster in Staphylococcus aureus CC398. Vet. Microbiol. 2015, 177:219-223.
39. Price L.B., Stegger M., Hasman H., Aziz M., Larsen J., Andersen P.S., Pearson T., Waters A.E., Foster J.T., Schupp J., Gillece J., Driebe E., Liu C.M., Springer B., Zdovc I., Battisti A., Franco A., Zmudzki J., Schwarz S., Butaye P., Jouy E., Pomba C., Porrero M.C., Ruimy R., Smith T.C., Robinson A., Weese J.S., Arriola C.S., Yu F., Lautend F., Keim P., Skov R., Aarestrup F.M. Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock. MBio 2012, 3:40305-40311.
40. 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.
41. Uhlemann A.C., Porcella S.F., Trivedi S., Sullivan S.B., Hafer C., Kennedy A.D., Barbian K.D., McCarthy A.J., Street C., Hirschberg D.L., Lipkin W.I., Lindsay J.A., DeLeo F.R., Lowy F.D. Identification of a highly transmissible animal-independent Staphylococcus aureus ST398 clone with distinct genomic and cell adhesion properties. MBio 2012, 3. (e00027-12).
42. Witte W., Braulke C., Cuny C., Strommenger B., Werner G., Heuck D., Jappe U., Wendt C., Linde H.J., Harmsen D. Emergence of methicillin-resistant Staphylococcus aureus with Panton-Valentine leukocidin genes in central Europe. Eur. J. Clin. Microbiol. Infect. Dis. 2005, 24:1-5.
43. McDougal L.K., Fosheim G.E., Nicholson A., Bulens S.N., Limbago B.M., Shearer J.E., Summers A.O., Patel J.B. Emergence of resistance among USA300 methicillin-resistant Staphylococcus aureus isolates causing invasive disease in the United States. Antimicrob. Agents Chemother. 2010, 54:3804-3811.
44. Argudín M.A., Tenhagen B.A., Fetsch A., Sachsenröder J., Käsbohrer A., Schroeter A., Hammerl J.A., Hertwig S., Helmuth R., Bräunig J., Mendoza M.C., Appel B., Rodicio M.R., Guerra B. Virulence and resistance determinants of German Staphylococcus aureus ST398 isolates from nonhuman sources. Appl. Environ. Microbiol. 2011, 77:3052-3060.
45. McCarthy A.J., Lindsay J.A. Staphylococcus aureus innate immune evasion is lineage-specific: a bioinfomatics study. Infect. Genet. Evol. 2013, 19:7-14.
46. Abbott Y., Leonard F.C., Markey B.B. Detection of three distinct genetic lineages in methicillin-resistant Staphylococcus aureus (MRSA) isolates from animals and veterinary personnel. Epidemiol. Infect. 2010, 138:764-767.
47. Garcia-Graells C., Antoine J., Larsen J., Catry B., Skov R., Denis O. Livestock veterinarians at high risk of acquiring methicillin-resistant Staphylococcus aureus ST398 Epidemiol Infect 2012, 140:383-389.
48. Wulf M.W., Sørum M., van Nes A., Skov R., Melchers W.J., Klaassen C.H., Voss A. Prevalence of methicillin-resistant Staphylococcus aureus among veterinarians: an international study. Clin. Microbiol. Infect. 2008, 14:29-34.
49. Layer F., Cuny C., Strommenger B., Werner G., Witte W. Current data and trends on methicillin-resistant Staphylococcus aureus (MRSA). Bundesgesundheitsblatt 2012, 55:1377-1386.
50. David M.Z., Taylor A., Lynfield R., Boxrud D.J., Short G., Zychowski D., Boyle-Vavra S., Daum R.S. Comparing pulsed-field gel electrophoresis with multilocus sequence typing, spa typing, staphylococcal cassette chromosome mec (SCCmec) typing, and PCR for panton-valentine leukocidin, arcA, and opp3 in methicillin-resistant Staphylococcus aureus isolates at a U.S. Medical Center. J. Clin. Microbiol. 2013, 51:814-819.
51. Kinnevey P.M., Shore A.C., Brennan G.I., Sullivan D.J., Ehricht R., Monecke S., Coleman D.C. Extensive genetic diversity identified among sporadic methicillin-resistant Staphylococcus aureus isolates recovered in Irish hospitals between 2000 and 2012. Antimicrob. Agents Chemother. 2014, 58:1907-1917.
52. Varshney A.K., Mediavilla J.R., Robiou N., Guh A., Wang X., Gialanella P., Levi M.H., Kreiswirth B.N., Fries B.C. Diverse enterotoxin gene profiles among clonal complexes of Staphylococcus aureus isolates from the Bronx, New York. Appl. Environ. Microbiol. 2009, 75:6839-6849.
53. Grundmann H., Aanensen D.M., van den Wijngaard C.C., Spratt B.G., Harmsen D., Friedrich A.W. European Staphylococcal Reference Laboratory Working Geographic distribution of Staphylococcus aureus causing invasive infections in Europe: a molecular-epidemiological analysis. PLoS Med. 2010, 7.
54. Grundmann H., Schouls L.M., Aanensen D.M., Pluister G.N., Tami A., Chlebowicz M., Glasner C., Sabat A.J., Weist K., Heuer O., Friedrich A.W. ESCMID Study Group on Molecular Epidemiological Markers; European Staphylococcal Reference Laboratory Working Group. The dynamic changes of dominant clones of Staphylococcus aureus causing bloodstream infections in the European region: results of a second structured survey. Euro Surveill. 2014, 19(49).
55. Harrison E.M., Paterson G.K., Holden M.T., Larsen J., Stegger M., Larsen A.R., Petersen A., Skov R.L., Christensen J.M., Bak Zeuthen A., Heltberg O., Harris S.R., Zadoks R.N., Parkhill J., Peacock S.J., Holmes M.A. Whole genome sequencing identifies zoonotic transmission of MRSA isolates with the novel mecA homologue mecC. EMBO Mol. Med. 2013, 5:509-515.
56. Weber S.G., Gold H.S., Hooper D.C., Karchmer A.W., Carmeli Y. Fluoroquinolones and the risk for methicillin-resistant Staphylococcus aureus in hospitalized patients. Emerg. Infect. Dis. 2003, 9:1415-1422.