MRSA colonization and infection among persons with occupational livestock exposure in Europe: Prevalence, preventive options and evidence

Veterinary Microbiology

Volumn 200, Issue , 2017, Pages 6-12

  Goerge, Tobias ^a   Lorenz, Marthe Barbara ^a   van Alen, Sarah ^a   Hübner, Nils Olaf ^b   Becker, Karsten ^a   Köck, Robin ^a  

^a UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^b Institute of Medical Diagnostics (IMD)   (Germany)

Author keywords

Risk; ST398; Staff

Indexed keywords

PSEUDOMONIC ACID;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL STRAIN; COMMUNITY ACQUIRED INFECTION; EUROPE; HEALTH HAZARD; HOSPITAL INFECTION; HUMAN; IN VITRO STUDY; INCIDENCE; INFECTION PREVENTION; LIVESTOCK; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS INFECTION; OCCUPATIONAL EXPOSURE; OCCUPATIONAL HAZARD; PREVALENCE; ANIMAL; BACTERIUM ADHERENCE; BOVINE; CATTLE DISEASE; CROSS INFECTION; DRUG EFFECTS; ISOLATION AND PURIFICATION; MICROBIOLOGY; OCCUPATIONAL HEALTH; PHYSIOLOGY; PIG; STAPHYLOCOCCAL INFECTIONS; SWINE DISEASE; TRANSMISSION; ZOONOSIS;

ANIMALS; BACTERIAL ADHESION; CATTLE; CATTLE DISEASES; COMMUNITY-ACQUIRED INFECTIONS; CROSS INFECTION; EUROPE; HUMANS; INCIDENCE; LIVESTOCK; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; OCCUPATIONAL EXPOSURE; OCCUPATIONAL HEALTH; PREVALENCE; STAPHYLOCOCCAL INFECTIONS; SWINE; SWINE DISEASES; ZOONOSES;

EID: 84949672211     PISSN: 03781135     EISSN: 18732542     Source Type: Journal    
DOI: 10.1016/j.vetmic.2015.10.027     Document Type: Article

References (76)

1. Albrich, W.C., Harbarth, S., Health-care workers: source, vector, or victim of MRSA?. Lancet Infect. Dis. 8 (2008), 289–301.
2. Antoci, E., Pinzone, M.R., Nunnari, G., Stefani, S., Cacopardo, B., Prevalence and molecular characteristics of methicillin-resistant Staphylococcus aureus (MRSA) among subjects working on bovine dairy farms. Infez. Med. 21 (2013), 125–129.
3. Aspiroz, C., Lozano, C., Vindel, A., Lasarte, J.J., Zarazaga, M., Torres, C., Skin lesion caused by ST398 and ST1 MRSA, Spain. Emerg. Infect. Dis. 16 (2010), 157–159.
4. Ballhausen, B., Jung, P., Kriegeskorte, A., Makgotlho, P.E., Ruffing, U., von Müller, L., Köck, R., Peters, G., Herrmann, M., Ziebuhr, W., Becker, K., Bischoff, M., LA-MRSA CC398 differ from classical community acquired-MRSA and hospital acquired-MRSA lineages: functional analysis of infection and colonization processes. Int. J. Med. Microbiol. 304 (2014), 777–786.
5. Berning, C., Lanckohr, C., Baumgartner, H., Drescher, M., Becker, K., Peters, G., Köck, R., Kahl, B.C., Fatal infections caused by methicillin-resistant Staphylococcus aureus of clonal complex 398: case presentations and molecular epidemiology. JMM Case Rep. 2 (2015), 1–4.
6. Bisdorff, B., Scholholter, J.L., Claussen, K., Pulz, M., Nowak, D., Radon, K., MRSA-ST398 in livestock farmers and neighbouring residents in a rural area in Germany. Epidemiol. Infect. 140 (2012), 1800–1808.
7. Camoez, M., Sierra, J.M., Pujol, M., Hornero, A., Martin, R., Dominguez, M.A., Prevalence and molecular characterization of methicillin-resistant Staphylococcus aureus ST398 resistant to tetracycline at a Spanish hospital over 12 years. PLoS One, 8, 2013, e72828.
8. Corne, P., Marchandin, H., Jonquet, O., Campos, J., Banuls, A.L., Molecular evidence that nasal carriage of Staphylococcus aureus plays a role in respiratory tract infections of critically ill patients. J. Clin. Microbiol. 43 (2005), 3491–3493.
9. Cox, L.A. Jr., Popken, D.A., Quantitative assessment of human MRSA risks from swine. Risk Anal. 34 (2014), 1639–1650.
10. 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, 4, 2009, e6800.
11. 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. 21 (2015), 750–757.
12. Dahms, C., Hübner, N.O., Cuny, C., Kramer, A., Occurrence of methicillin-resistant Staphylococcus aureus in farm workers and the livestock environment in Mecklenburg-Western Pomerania, Germany. Acta Vet. Scand., 56, 2014, 53.
13. Declercq, P., Petre, D., Gordts, B., Voss, A., Complicated community-acquired soft tissue infection by MRSA from porcine origin. Infection 36 (2008), 590–592.
14. Deiters, C., Günnewig, V., Friedrich, A.W., Mellmann, A., Köck, R., Are cases of Methicillin-resistant Staphylococcus aureus clonal complex (CC) 398 among humans still livestock-associated?. Int. J. Med. Microbiol. 305 (2015), 110–113.
15. Dorado-Garcia, A., Bos, M.E., Graveland, H., Van Cleef, B.A., Verstappen, K.M., Kluytmans, J.A., Wagenaar, J.A., Heederik, D.J., Risk factors for persistence of livestock-associated MRSA and environmental exposure in veal calf farmers and their family members: an observational longitudinal study. BMJ Open, 3, 2013, e003272.
16. Fanoy, E., Helmhout, L.C., van der Vaart, W.L., Weijdema, K., van Santen-Verheuvel, M.G., Thijsen, S.F., de Neeling, A.J., van Wamel, W.J., Manaskova, S.H., Kingma-Thijssen, J.L., An outbreak of non-typeable MRSA within a residential care facility. Euro Surveill., 14, 2009 pii 19080.
17. 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. 140 (2012), 383–389.
18. Geenen, P.L., Graat, E.A., Haenen, A., Hengeveld, P.D., Van Hoek, A.H., Huijsdens, X.W., Kappert, C.C., Lammers, G.A., Van Duijkeren, E., Van De Giessen, A.W., Prevalence of livestock-associated MRSA on Dutch broiler farms and in people living and/or working on these farms. Epidemiol. Infect. 141 (2013), 1099–1108.
19. Gilbert, M.J., Bos, M.E., Duim, B., Urlings, B.A., Heres, L., Wagenaar, J.A., Heederik, D.J., Livestock-associated MRSA ST398 carriage in pig slaughterhouse workers related to quantitative environmental exposure. Occup. Environ. Med. 69 (2012), 472–478.
20. Golding, G.R., Bryden, L., Levett, P.N., McDonald, R.R., Wong, A., Wylie, J., Graham, M.R., Tyler, S., Van Domselaar, G., Simor, A.E., Gravel, D., Mulvey, M.R., Livestock-associated methicillin-resistant Staphylococcus aureus sequence type 398 in humans, Canada. Emerg. Infect. Dis. 16 (2010), 587–594.
21. Graveland, H., Wagenaar, J.A., Heesterbeek, H., Mevius, D., van Duijkeren, E., Heederik, D., Methicillin resistant Staphylococcus aureus ST398 in veal calf farming: human MRSA carriage related with animal antimicrobial usage and farm hygiene. PLoS One, 5, 2010, e10990.
22. Graveland, H., Wagenaar, J.A., Bergs, K., Heesterbeek, H., Heederik, D., Persistence of livestock associated MRSA CC398 in humans is dependent on intensity of animal contact. PLoS One, 6, 2011, e16830.
23. Grisold, A.J., Zarfel, G., Hoenigl, M., Krziwanek, K., Feierl, G., Masoud, L., Leitner, E., Wagner-Eibel, U., Badura, A., Marth, E., Occurrence and genotyping using automated repetitive-sequence-based PCR of methicillin-resistant Staphylococcus aureus ST398 in Southeast Austria. Diagn. Microbiol. Infect. Dis. 66 (2010), 217–221.
24. Hartmeyer, G.N., Gahrn-Hansen, B., Skov, R.L., Kolmos, H.J., Pig-associated methicillin-resistant Staphylococcus aureus: family transmission and severe pneumonia in a newborn. Scand. J. Infect. Dis. 42 (2010), 318–320.
25. 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. Antimicrob., 5, 2006, 26.
26. Idelevich, E.A., Lanckohr, C., Horn, D., Wieler, L.H., Becker, K., Köck, R., (2015). [Multidrug-resistant bacteria in Germany: the impact of sources outside healthcare facilities]. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz. Oct 7. [Epub ahead of print].
27. Jurke, A., Köck, R., Becker, K., Thole, S., Hendrix, R., Rossen, J., Daniels-Haardt, I., Friedrich, A., Reduction of the nosocomial meticillin-resistant Staphylococcus aureus incidence density by a region-wide search and follow-strategy in forty German hospitals of the EUREGIO, 2009 to 2011. Euro Surveill., 18, 2013 pii 20579.
28. Köck, R., Harlizius, J., Bressan, N., Laerberg, R., Wieler, L.H., Witte, W., Deurenberg, R.H., Voss, A., Becker, K., Friedrich, A.W., Prevalence and molecular characteristics of methicillin-resistant Staphylococcus aureus (MRSA) among pigs on German farms and import of livestock-related MRSA into hospitals. Eur. J. Clin. Microbiol. Infect. Dis. 28 (2009), 1375–1382.
29. Köck, R., Loth, B., Koksal, M., Schulte-Wulwer, J., Harlizius, J., Friedrich, A.W., Persistence of nasal colonization with livestock-associated methicillin-resistant Staphylococcus aureus in pig farmers after holidays from pig exposure. Appl. Environ. Microbiol. 78 (2012), 4046–4047.
30. Köck, R., Schaumburg, F., Mellmann, A., Koksal, 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, 8, 2013, e55040.
31. Köck, R., Ballhausen, B., Bischoff, M., Cuny, C., Eckmanns, T., Fetsch, A., Harmsen, D., Goerge, T., Oberheitmann, B., Schwarz, S., Selhorst, T., Tenhagen, B.A., Walther, B., Witte, W., Ziebuhr, W., Becker, K., The burden of zoonotic MRSA colonization and infection in Germany. Berl. Munch. Tierarztl. Wochenschr. 127 (2014), 384–398.
32. Köck, R., Becker, K., Cookson, B., van Gemert-Pijnen, J., Harbarth, S., Kluytmans, J., Mielke, M., Peters, G., Skov, R., Struelens, M., Tacconelli, E., Witte, W., Friedrich, A., Systematic literature analysis and review of targeted preventive measures to limit healthcare-associated infections by meticillin-resistant Staphylococcus aureus. Euro Surveill., 19, 2014 pii 20860.
33. Kaspar, U., Kriegeskorte, A., Schubert, T., Peters, G., Rudack, C., Pieper, D.H., Wos-Oxley, M., Becker, K., The culturome of the human nose habitats reveals individual bacterial fingerprint patterns. Environ. Microbiol., 2015, 10.1111/1462-2920.12891 Epub ahead of print.
34. Kluytmans, J., van Belkum, A., Verbrugh, H., Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin. Microbiol. Rev. 10 (1997), 505–520.
35. Kommission für Krankenhaushygiene und Infektionsprävention (KRINKO), Empfehlungen zur Prüvention und Kontrolle von Methicillinresistenten Staphylococcus aureus-Stümmen (MRSA) in medizinischen und pflegerischen Einrichtungen. Bundesgesundheitsbl 57 (2014), 696–732.
36. Krziwanek, K., Metz-Gercek, S., Mittermayer, H., Methicillin-Resistant Staphylococcus aureus ST398 from human patients, upper Austria. Emerg. Infect. Dis. 15 (2009), 766–769.
37. Layer, F., Werner, G., Eigenschaften, Häufigkeit und Verbreitung von MRSA in Deutschland –Update 2011/2012. EpiBull 21 (2013), 187–193.
38. Lekkerkerk, W.S., van de Sande-Bruinsma, N., van der Sande, M.A., Tjon, A.T.A., Groenheide, A., Haenen, A., Timen, A., van den Broek, P.J., van Wamel, W.J., de Neeling, A.J., Richardus, J.H., Verbrugh, H.A., Vos, M.C., Emergence of MRSA of unknown origin in the Netherlands. Clin. Microbiol. Infect. 18 (2012), 656–661.
39. Lozano, C., Aspiroz, C., Ara, M., Gomez-Sanz, E., Zarazaga, M., Torres, C., Methicillin-resistant Staphylococcus aureus (MRSA) ST398 in a farmer with skin lesions and in pigs of his farm: clonal relationship and detection of lnu(A) gene. Clin. Microbiol. Infect. 17 (2011), 923–927.
40. Lozano, C., Aspiroz, C., Charlez, L., Gomez-Sanz, E., Toledo, M., Zarazaga, M., Torres, C., Skin lesion by methicillin-resistant Staphylococcus aureus ST398-t1451 in a Spanish pig farmer: possible transmission from animals to humans. Vector Borne Zoonotic Dis. 11 (2011), 605–607.
41. Lozano, C., Aspiroz, C., Ezpeleta, A.I., Gomez-Sanz, E., Zarazaga, M., Torres, C., Empyema caused by MRSA ST398 with atypical resistance profile, Spain. Emerg. Infect. Dis. 17 (2011), 138–140.
42. Lozano, C., Aspiroz, C., Lasarte, J.J., Gomez-Sanz, E., Zarazaga, M., Torres, C., Dynamic of nasal colonization by methicillin-resistant Staphylococcus aureus ST398 and ST1 after mupirocin treatment in a family in close contact with pigs. Comp. Immunol. Microbiol. Infect. Dis. 34 (2011), e1–e7.
43. Lozano, C., Rezusta, A., Gomez, P., Gomez-Sanz, E., Baez, N., Martin-Saco, G., Zarazaga, M., Torres, C., High prevalence of spa types associated with the clonal lineage CC398 among tetracycline-resistant methicillin-resistant Staphylococcus aureus strains in a Spanish hospital. J. Antimicrob. Chemother. 67 (2012), 330–334.
44. Meyer, V., Kerk, N., Mellmann, A., Friedrich, A., Luger, T.A., Goerge, T., MRSA eradication in dermatologic outpatients-theory and practice. J. Dtsch. Dermatol. Ges. 10 (2012), 186–196.
45. Mielke, M., Bölt, U., Geffers, C., Basisdaten der stationären Krankenversorgung in Deutschland-nosokomiale Infektionen. EpiBull 36 (2010), 359–368.
46. Monaco, M., Pedroni, P., Sanchini, A., Bonomini, A., Indelicato, A., Pantosti, A., Livestock-associated methicillin-resistant Staphylococcus aureus responsible for human colonization and infection in an area of Italy with high density of pig farming. BMC Infect. Dis., 13, 2013, 258.
47. Morcillo, A., Castro, B., González, J., Rodriguez-Alvarez, C., Novo, M., Sierra, A., Arias, A. (2011). High prevalence of methicillin-resistant Staphylococcus aureus in pigs and slaughterhouse workers (P900). In: 21st European Congress of Clinical Microbiology and Infectious Diseases (ECCMID), Milano, 07.05.-10.05.2011.
48. Mulders, M.N., Haenen, A.P., Geenen, P.L., Vesseur, P.C., Poldervaart, E.S., Bosch, T., Huijsdens, X.W., Hengeveld, P.D., Dam-Deisz, W.D., Graat, E.A., Mevius, D., Voss, A., Van De Giessen, A.W., Prevalence of livestock-associated MRSA in broiler flocks and risk factors for slaughterhouse personnel in The Netherlands. Epidemiol. Infect. 138 (2010), 743–755.
49. Nathaus, R., Schulz, J., Hartung, J., Cuny, C., Fetsch, A., Blaha, T., Meemken, D., [Investigations into the use of respiratory masks for reducing the MRSA-exposure of veterinarians visiting regularly pig herds-first experiences]. Berl. Munch. Tierarztl. Wochenschr. 124 (2011), 128–135.
50. Nicholson, T.L., Shore, S.M., Smith, T.C., Frana, T.S., Livestock-associated methicillin-resistant Staphylococcus aureus (LA-MRSA) isolates of swine origin form robust biofilms. PLoS One, 8, 2013, e73376.
51. Omland, O., Hoffmann, L., Occupational acquisition of methicillin-resistant Staphylococcus aureus in humans–a description of MRSA carrier and infected cases from the Region of North Jutland in Denmark. Ann. Agric. Environ. Med. 19 (2012), 637–640.
52. 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. 15 (2009), 845–847.
53. Paterson, G.K., Harrison, E.M., Craven, E.F., Petersen, A., Larsen, A.R., Ellington, M.J., Torok, M.E., Peacock, S.J., Parkhill, J., Zadoks, R.N., Holmes, M.A., Incidence and characterisation of methicillin-resistant Staphylococcus aureus (MRSA) from nasal colonisation in participants attending a cattle veterinary conference in the UK. PLoS One, 8, 2013, e68463.
54. Richter, A., Sting, R., Popp, C., Rau, J., Tenhagen, B.A., Guerra, B., Hafez, H.M., Fetsch, A., Prevalence of types of methicillin-resistant Staphylococcus aureus in turkey flocks and personnel attending the animals. Epidemiol. Infect. 140 (2012), 2223–2232.
55. Ruhlmann, C.H., Kolmos, H.J., Kristiansen, J.E., Skov, R., Pigs as an infection source for methicillin resistant Staphylococcus aureus infections in humans. Ugeskr. Laeger, 170, 2008, 3436.
56. Slingerland, B.C., Tavakol, M., McCarthy, A.J., Lindsay, J.A., Snijders, S.V., Wagenaar, J.A., van Belkum, A., Vos, M.C., Verbrugh, H.A., van Wamel, W.J., Survival of Staphylococcus aureus ST398 in the human nose after artificial inoculation. PLoS One, 7, 2012, e48896.
57. Smith, T.C., Wardyn, S.E., Human Infections with Staphylococcus aureus CC398. Curr. Environ. Health Rep. 2 (2015), 41–51.
58. 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. 16 (2010), 346–348.
59. Statens Serum Institut, National Veterinary Institute, Technical University of Denmark, National Food Institute, Technical University of Denmark 2014. DANMAP 2013—Use of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from food animals, food and humans in Denmark.
60. Van Cleef, B.A., Broens, E.M., Voss, A., Huijsdens, X.W., Zuchner, L., Van Benthem, B.H., Kluytmans, J.A., Mulders, M.N., Van De Giessen, A.W., High prevalence of nasal MRSA carriage in slaughterhouse workers in contact with live pigs in The Netherlands. Epidemiol. Infect. 138 (2010), 756–763.
61. Van Cleef, B.A., Verkade, E.J., Wulf, M.W., Buiting, A.G., Voss, A., Huijsdens, X.W., van Pelt, W., Mulders, M.N., Kluytmans, J.A., Prevalence of livestock-associated MRSA in communities with high pig-densities in The Netherlands. PLoS One, 5, 2010, e9385.
62. Van Cleef, B.A., Graveland, H., Haenen, A.P., van de Giessen, A.W., Heederik, D., Wagenaar, J.A., Kluytmans, J.A., Persistence of livestock-associated methicillin-resistant Staphylococcus aureus in field workers after short-term occupational exposure to pigs and veal calves. J. Clin. Microbiol. 49 (2011), 1030–1033.
63. Van Cleef, B.A., van Benthem, B.H., Haenen, A.P., Bosch, T., Monen, J., Kluytmans, J.A., Low incidence of livestock-associated methicillin-resistant Staphylococcus aureus bacteraemia in The Netherlands in 2009. PLoS One, 8, 2013, e73096.
64. Van Cleef, B.A., van Benthem, B.H., Verkade, E.J., van Rijen, M., Kluytmans-van den Bergh, M.F., Schouls, L.M., Duim, B., Wagenaar, J.A., Graveland, H., Bos, M.E., Heederik, D., Kluytmans, J.A., Dynamics of methicillin-resistant Staphylococcus aureus and methicillin-susceptible Staphylococcus aureus carriage in pig farmers: a prospective cohort study. Clin. Microbiol. Infect. 20 (2014), O764–O771.
65. Van De Griend, P., Herwaldt, L.A., Alvis, B., DeMartino, M., Heilmann, K., Doern, G., Winokur, P., Vonstein, D.D., Diekema, D., Community-associated methicillin-resistant Staphylococcus aureus, Iowa, USA. Emerg. Infect. Dis. 15 (2009), 1582–1589.
66. Van Den Broek, I., Van Cleef, B., Haenen, A., Broens, E., Van Der Wolf, P., Van Den Broek, M., Huijsdens, X., Kluytmans, J., Van De Giessen, A., Tiemersma, E., Methicillin-resistant Staphylococcus aureus in people living and working in pig farms. Epidemiol. Infect. 137 (2009), 700–708.
67. Vandendriessche, S., Vanderhaeghen, W., Soares, F.V., Hallin, M., Catry, B., Hermans, K., Butaye, P., Haesebrouck, F., Struelens, M.J., Denis, O., Prevalence, risk factors and genetic diversity of methicillin-resistant Staphylococcus aureus carried by humans and animals across livestock production sectors. J. Antimicrob. Chemother. 68 (2013), 1510–1516.
68. Verkade, E., Bosch, T., Hendriks, Y., Kluytmans, J., Outbreak of methicillin-resistant Staphylococcus aureus ST398 in a Dutch nursing home. Infect. Control Hosp. Epidemiol. 33 (2012), 624–626.
69. Verkade, E., van Benthem, B., den Bergh, M.K., van Cleef, B., van Rijen, M., Bosch, T., Kluytmans, J., Dynamics and determinants of Staphylococcus aureus carriage in livestock veterinarians: a prospective cohort study. Clin. Infect. Dis. 57 (2013), e11–e17.
70. Witte, W., Strommenger, B., Stanek, C., Cuny, C., Methicillin-resistant Staphylococcus aureus ST398 in humans and animals, Central Europe. Emerg. Infect. Dis. 13 (2007), 255–258.
71. 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. 12 (2006), 1939–1941.
72. Wulf, M.W., Markestein, A., van der Linden, F.T., Voss, A., Klaassen, C., Verduin, C.M., First outbreak of methicillin-resistant Staphylococcus aureus ST398 in a Dutch hospital, June 2007. Euro Surveill., 13, 2008 pii 8051.
73. Wulf, M.W., Sorum, 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. 14 (2008), 29–34.
74. Wulf, M.W., Verduin, C.M., van Nes, A., Huijsdens, X., Voss, A., Infection and colonization with methicillin resistant Staphylococcus aureus ST398 versus other MRSA in an area with a high density of pig farms. Eur. J. Clin. Microbiol. Infect. Dis. 31 (2012), 61–65.
75. Zarb, P., Coignard, B., Griskeviciene, J., Muller, A., Vankerckhoven, V., Weist, K., Goossens, M., Vaerenberg, S., Hopkins, S., Catry, B., Monnet, D., Goossens, H., Suetens, C., National Contact Points for the, E.p.p.p.s., Hospital Contact Points for the, E.p.p.p.s., 2012. The European Centre for Disease Prevention and Control (ECDC) pilot point prevalence survey of healthcare-associated infections and antimicrobial use. Euro Surveill., 2012, 17.
76. von Eiff, C., Becker, K., Machka, K., Stammer, H., Peters, G., Study Group, 2001. Nasal carriage as a source of Staphylococcus aureus bacteremia. N. Engl. J. Med. 344 (2001), 11–16.