Staphylococcus aureus and surgical site infections: benefits of screening and decolonization before surgery

Journal of Hospital Infection

Volumn 94, Issue 3, 2016, Pages 295-304

  Humphreys, H ^a,b   Becker, K ^c   Dohmen, P M ^d,e   Petrosillo, N ^f   Spencer, M ^g   van Rijen, M ^h   Wechsler Fordos A ⁱ   Pujol, M ^j   Dubouix, A ^k   Garau, J ^l  

^a ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^b BEAUMONT HOSPITAL   (Ireland)

^c UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^d HUMBOLDT UNIVERSITY   (Germany)

^e UNIVERSITY OF THE FREE STATE   (South Africa)

^f NATIONAL INSTITUTE FOR INFECTIOUS DISEASES L SPALLANZANI   (Italy)

^g Department of Quality and Patient Safety   (United States)

^h Laboratory for Microbiology and Infection Control   (Netherlands)

ⁱ KRANKENANSTALT RUDOLFSTIFTUNG   (Austria)

^j HOSPITAL UNIVERSITARI DE BELLVITGE   (Spain)

^k Clinique de l Union   (France)

^l Mutua de Terassa University Hospital   (Spain)

more..

Author keywords

Decolonization; MRSA; Screening; Staphylococcus aureus; Surgical site infection prevention

Indexed keywords

BIOCIDE; PSEUDOMONIC ACID; ANTIINFECTIVE AGENT;

ANTIBIOTIC PROPHYLAXIS; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; BACTERIAL COLONIZATION; BACTERIAL DECOLONIZATION; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM CULTURE; BACTERIUM DETECTION; BACTERIUM ISOLATE; CATHETER INFECTION; COAGULASE NEGATIVE STAPHYLOCOCCUS; GENE SEQUENCE; HOSPITALIZATION; HUMAN; MASS SCREENING; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; METHICILLIN SUSCEPTIBLE STAPHYLOCOCCUS AUREUS; MOLECULAR CLONING; MYOSITIS; NECROTIZING FASCIITIS; NECROTIZING MYOSITIS; NECROTIZING PNEUMONIA; NONHUMAN; PNEUMONIA; POLYMERASE CHAIN REACTION; POPULATION STRUCTURE; PREOPERATIVE PERIOD; PSEUDOMONAS FLUORESCENS; QACA GENE; QACB GENE; REVIEW; STAPHYLOCOCCUS EPIDERMIDIS; STAPHYLOCOCCUS INFECTION; SURGICAL INFECTION; HETEROZYGOTE; ISOLATION AND PURIFICATION; MICROBIOLOGY; PROCEDURES; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; SURGICAL WOUND INFECTION;

ANTI-BACTERIAL AGENTS; CARRIER STATE; HUMANS; MASS SCREENING; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; SURGICAL WOUND INFECTION;

EID: 84994691780     PISSN: 01956701     EISSN: 15322939     Source Type: Journal    
DOI: 10.1016/j.jhin.2016.06.011     Document Type: Review

References (107)

1. 1 Klevens, R.M., Edwards, J.R., Richards, C.L. Jr., et al. Estimated health care-associated infections and death in US hospitals, 2002. Public Health Rep 122 (2007), 160–166.
2. 2 Allegranzi, B., Bagheri Nejad, S., Combescure, C., et al. Burden of endemic health-care-associated infection in developing countries: systemic review and meta-analysis. Lancet 377 (2011), 228–241.
3. 3 European Centre for Disease Prevention and Control, Annual epidemiological report on communicable disease in Europe 2008: report on the state of communicable disease in the EU and EEA/EFTA countries., 2008, ECDC, Solna Available at: http://www.ecdc.europa.eu/en/publications/Publications/0812_SUR_Annual_Epidemiological_Report_2008.pdf [last accessed September 2015].
4. 4 Jenks, P.J., Laurent, M., McQuarry, S., Watkins, R., Clinical and economic burden of surgical site infection (SSI) and predicted financial consequences of elimination of SSI from an English hospital. J Hosp Infect 86 (2014), 24–33.
5. 5 Kim, D.H., Spencer, M., Davidson, S.M., et al. Institutional prescreening for detection and eradication of methicillin-resistant Staphylococcus aureus in patients undergoing elective orthopaedic surgery. J Bone Joint Surg Am 92 (2010), 1820–1826.
6. 6 Gaynes, R.P., Culver, D.H., Horan, T.C., Edwards, J.R., Richards, C., Tolson, J.S., Surgical site infections (SSI) rates in the United States, 1992–1998: the National Nosocomial Infection Surveillance System basic SSI risk index. Clin Infect Dis 33 (2001), S69–S77.
7. 7 Gastmeier, P., Geffers, C., Brandt, C., et al. Effectiveness of a nationwide nosocomial infection surveillance system for reducing nosocomial infections. J Hosp Infect 64 (2006), 16–22.
8. 8 Dohmen, P.M., Economic burden of surgical site infections in cardiac surgery. J Med Microb Diagn, 2, 2013, 3.
9. 9 Dohmen, P.M., Antibiotic resistance in common pathogens reinforces the need to minimize surgical site infections. J Hosp Infect 70 (2008), S15–S20.
10. 10 Healthcare Infection Control Practices Advisory Committee, Draft guideline for the prevention of surgical site infection. 2014, Centers for Disease Prevention and Control, Atlanta, GA.
11. 11 Anderson, D.J., Kaye, K.S., Chen, L.F., et al. Clinical and financial outcomes due to methicillin-resistant Staphylococcus surgical site infection: a multi-center matched outcomes study. Plos One, 4, 2009, e8305.
12. 12 Perencevich, E.N., Sands, K.E., Cosgrove, S.E., Guadagnoli, E., Meara, E., Platt, R., Health and economic impact of surgical site infections diagnosed after hospital discharge. Emerg Infect Dis 9 (2003), 196–203.
13. 13 Schweizer, M., Perencevich, E., McDanel, J., et al. Effectiveness of a bundled intervention of decolonization and prophylaxis to decrease Gram-positive surgical site infections after cardiac or orthopedic surgery: systematic review and meta-analysis. BMJ, 346, 2013, f2743.
14. 14 Calfee, D.P., Considering universal mupirocin decolonization as an option for preventing surgical site infections. Clin Infect Dis 62 (2016), 637–639.
15. 15 Lindsay, J.A., Holden, T.G., Staphylococcus aureus: superbug, super genome?. Trends Microbiol 8 (2004), 378–385.
16. 16 David, M.Z., Daum, R.S., Bayer, A.S., et al. Staphylococcus aureus bacteraemia at 5 US academic medical centres, 2008–2011: significant geographic variation in community-onset infections. Clin Infect Dis 59 (2014), 798–807.
17. 17 Feil, E.J., Cooper, J.E., Grundnann, H., et al. How clonal is Staphylococcus aureus?. J Bacteriol 185 (2003), 3307–3316.
18. 18 Campbell, S.J., Deshmukh, H.S., Nelson, C.L., et al. Genotypic characteristics of Staphylococcus aureus isolates from a multinational trial of complicated skin and skin structre infections. J Clin Microbiol 46 (2008), 678–684.
19. 19 Grundmann, H., Aanensen, D.M., van den Wijngaard, C.C., Spratt, B.G., Harmsen, D., Friedrich, A.W., Geographic distribution of Staphylococcus aureus causing invasive infections in Europe: a molecular-epidemiological analysis. PLos Med, 7, 2010, e1000215.
20. 20 European Centre for Disease Prevention and Control, Annual epidemiological report 2014. Antimicrobial resistance and healthcare-associated infections., 2015, ECDC, Solna.
21. 21 Johnson, N.B., Hayes, L.D., Brown, K., Hoo, E.C., Ethier, K.A., CDC national health report: leading causes of morbidity and mortality and associated behavioral risk and protective factors – United States, 2005–2013. MMWR Surveill Summ 63:Suppl. 4 (2014), 3–27.
22. 22 Woodford, N., Livermore, D.M., Infections caused by Gram-positive bacteria: a review of the global challenge. J Infect 59:Suppl. 1 (2009), S4–S16.
23. 23 Schaumburg, F., Alabi, A.S., Peters, G., Becker, K., New epidemiology of Staphylococcus aureus infection in Africa. Clin Microbiol Infect 20 (2014), 589–596.
24. 24 Grundmann, H., Schouls, L.M., Aanensen, D.M., et al. The dynamic changes of dominant clones of Staphylococcus aureus causing bloodstream infections in the European region: results of a second structured survey. EuroSurveill, 19, 2014, pii:20987.
25. 25 Monecke, S., Coombs, G., Shore, A.C., et al. A field guide to pandemic, epidemic and sporadic clones of methicillin-resistant Staphylococcus aureus. PLoS One, 6, 2011, e17936.
26. 26 Jurke, A., Köck, R., Becker, K., et al. Molecular epidemiology of meticillin-resistant Staphylococcus aureus (MRSA): think regionally but use globally uniform typing languages. EuroSurveill, 18, 2013, pii:20617.
27. 27 Okon, K.O., Shittu, A.O., Kudi, A.A., Umar, H., Becker, K., Schaumburg, F., Population dynamics of Staphylococcus aureus from Northeastern Nigeria in 2007 and 2012. Epidemiol Infect 142 (2014), 1737–1740.
28. 28 Schaumburg, F., Köck, R., Mellmann, A., et al. Population dynamics among methicillin resistant Staphylococcus aureus in Germany during a 6-year period. J Clin Microbiol 50 (2012), 3186–3192.
29. 29 Nimmo, G.R., USA300 abroad: global spread of a virulent strain of community-associated methicillin-resistant Staphylococcus aureus. Clin Microbiol Infect 18 (2012), 725–734.
30. 30 Tenover, F.C., Goering, R.V., Methicillin-resistant Staphylococcus aureus strain USA300: origin and epidemiology. J Antimicrob Chemother 64 (2009), 441–446.
31. 31 Köck, R., Schaumburg, F., Mellmann, A., et al. Livestock-associated methicillin-resistant Staphylococcus aureus (MRSA) as causes of human infection and colonization in Germany. PLoS One, 8, 2013, e55040.
32. 32 van Cleef, B.A., Monnet, D.L., Voss, A., et al. Livestock-associated methicillin-resistant Staphylococcus aureus in humans, Europe. Emerg Infect Dis 17 (2011), 502–505.
33. 33 Shore, A.C., Coleman, D.C., Staphylococcal cassette chromosome mec: recent advances and new insights. IntJ Med Microbiol 303 (2013), 350–359.
34. 34 Becker, K., Ballhausen, B., Köck, R., Kriegeskorte, A., Methicillin resistance in Staphylococcus isolates: the ‘mec alphabet’ with specific consideration of mecC, a mec homolog associated with zoonotic S. aureus lineages. Int J Med Microbiol 304 (2014), 794–804.
35. 35 Miller, L.G., Perdreau-Remington, F., Rieg, G., et al. Necrotizing fasciitis caused by community-associated methicillin-resistant Staphylococcus aureus in Los Angeles. N Engl J Med 352 (2005), 1445–1453.
36. 36 Gillet, Y., Issartel, B., Vanhems, P., et al. Association between Staphylococcus aureus strains carrying gene for Panton-Valentine leukocidin and highly lethal necrotising pneumonia in young immunocompetent patients. Lancet 359 (2002), 753–759.
37. 37 Dufour, P., Gillet, Y., Bes, M., et al. Community-acquired methicillin-resistant Staphylococcus aureus infections in France: emergence of a single clone that produces Panton-Valentine leukocidin. Clin Infect Dis 35 (2002), 819–824.
38. 38 Köck, R., Harlizius, J., Bressan, N., et al. 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.
39. 39 Köck, R., Siam, K., Al-Malat, S., et al. Characteristics of hospital patients colonized with livestock-associated meticillin-resistant Staphylococcus aureus (MRSA) CC398 versus other MRSA clones. J Hosp Infect 79 (2011), 292–296.
40. 40 Price LB, Stegger M, Hasman H, et al. Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock. MBio 2012;3:pii:e00305–e0011.
41. 41 van Cleef, B.A., Verkade, E.J., Wulf, M.W., et al. Prevalence of livestock-associated MRSA in communities with high pig-densities in The Netherlands. PLoS One, 5, 2010, e9385.
42. 42 Kommission für Krankenhaushygiene und Infektionsprävention (KRINKO) beim Robert Koch-Institut, Empfehlungen zur Prävention und Kontrolle von Methicillin-resistenten Staphylococcus aureus-Stämmen (MRSA) in medizinischen und pflegerischen Einrichtungen. Empfehlung der Kommission für Krankenhaushygiene und Infektionsprävention (KRINKO) beim Robert Koch-Institut. Bundesgesundheitsbl Gesundheitsforsch Gesundheitsschutz 57 (2014), 696–732.
43. 43 Lekkerkerk, W.S., van Wamel, W.J., Snijders, S.V., et al. What is the origin of livestock-associated methicillin-resistant Staphylococcus aureus clonal complex 398 isolates from humans without livestock contact? An epidemiological and genetic analysis. J Clin Microbiol 53 (2015), 1836–1841.
44. 44 García-Álvarez, M., Holden, M.T., Lindsay, H., et al. Meticillin-resistant Staphylococcus aureus with a novel mecA homologue in human and bovine populations in the UK and Denmark: a descriptive study. Lancet Infect Dis 11 (2011), 595–603.
45. 45 Shore, A.C., Deasy, E.C., Slickers, P., et al. Detection of staphylococcal cassette chromosome mec type XI encoding highly divergent mecA, mecI, mecR1, blaZ and ccr genes in human clinical clonal complex 130 methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 55 (2011), 3765–3773.
46. 46 Ballhausen, B., Kriegeskorte, A., Schleimer, N., Peters, G., Becker, K., The mecA homolog mecC confers resistance against β-lactams in Staphylococcus aureus irrespective of the genetic strain background. Antimicrob Agents Chemother 58 (2014), 3791–3798.
47. 47 Becker, K., Larsen, A.R., Skov, R.L., et al. Evaluation of a modular multiplex-PCR methicillin-resistant Staphylococcus aureus (MRSA) detection assay adapted for mecC detection. J Clin Microbiol 51 (2013), 1917–1919.
48. LGA251, is present in methicillin-resistant Staphylococcus aureus isolates from a diverse range of host species. J Antimicrob Chemother 67 (2012), 2809–2813.
49. 49 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, 6, 2011, e24360.
50. 50 Kriegeskorte, A., Ballhausen, B., Idelevich, E.A., et al. Human MRSA isolates with novel genetic homolog, Germany. Emerg Infect Dis 18 (2012), 1016–1018.
51. 51 Loncaric, I., Kübber-Heiss, A., Posautz, A., et al. Characterization of methicillin-resistant Staphylococcus spp. carrying the mecC gene, isolated from wildlife. J AntimicrobChemother 68 (2013), 2222–2225.
52. 52 Walther, B., Wieler, L.H., Vincze, S., et al. MRSA variant in companion animals. Emerg Infect Dis 18 (2012), 2017–2020.
53. 53 Kavi, J., Andrews, J.M., Wise, R., Mupirocin-resistant Staphylococcus aureus. Lancet, 330, 1987, 1472.
54. 54 Udo, E.E., Jacob, L.E., Mathew, B., Genetic analysis of methicillin-resistant Staphylococcus aureus expressing high- and low-level mupirocin resistance. J Med Microbiol 50 (2001), 909–915.
55. 55 Singh, A., Karimpour-Fard, A., Gill, R.T., Increased mutation frequency in redox-impaired Escherichia coli due to RelA- and RpoS-mediated repression of DNA repair. Appl Environ Microbiol 76 (2010), 5463–5470.
56. 56 Patel, J.B., Gorwitz, R.J., Jernigan, J.A., Mupirocin resistance. Clin Infect Dis 49 (2009), 935–941.
57. 57 Morton, T.M., Johnston, J.L., Patterson, J., Archer, G.L., Characterization of a conjugative staphylococcal mupirocin resistance plasmid. Antimicrob Agents Chemother 39 (1995), 1272–1280.
58. 58 Pérez-Roth, E., López-Aguilar, C., Alcoba-Florez, J., Méndez-Álvarez, S., High-level mupirocin resistance within methicillin-resistant Staphylococcus aureus pandemic lineages. Antimicrob Agents Chemother 50 (2006), 3207–3211.
59. 59 Hurdle, J.G., O'Neill, A.J., Mody, L., Chopra, I., Bradley, S.F., In vivo transfer of high-level mupirocin resistance from Staphylococcus epidermidis to methicillin-resistant Staphylococcus aureus associated with failure of mupirocin prophylaxis. J Antimicrob Chemother 56 (2005), 1166–1168.
60. 60 Hetem, D.J., Bootsma, M.C., Bonten, M.J., Prevention of surgical site infections: decontamination with mupirocin based on preoperative screening for Staphylococcus aureus carriers or universal decontamination?. Clin Infect Dis 62 (2016), 631–636.
61. 61 Pérez-Roth, E., Kwong, S.M., Alcoba-Florez, J., Firth, N., Méndez-Álvarez, S., Complete nucleotide sequence and comparative analysis of pPR9, a 41.7-kilobase conjugative staphylococcal multiresistance plasmid conferring high-level mupirocin resistance. Antimicrob Agents Chemother 54 (2010), 2252–2257.
62. 62 Lee, A.S., Macedo-Vinas, M., Francois, P., et al. Trends in mupirocin resistance in meticillin-resistant Staphylococcus aureus and mupirocin consumption at a tertiary care hospital. J Hosp Infect 77 (2011), 360–362.
63. 63 Bathoorn, E., Hetem, D.J., Alphenaar, J., Kusters, J.G., Bonten, M.J., Emergence of high-level mupirocin resistance in coagulase-negative staphylococci associated with increased short-term mupirocin use. J Clin Microbiol 50 (2012), 2947–2950.
64. 64 Desroches, M., Potier, J., Laurent, F., Bourrel, A.S., Doucet-Populaire, F., Decousser, J.W., Prevalence of mupirocin resistance among invasive coagulase-negative staphylococci and methicillin-resistant Staphylococcus aureus (MRSA) in France: emergence of a mupirocin-resistant MRSA clone harbouring mupA. J Antimicrob Chemother 68 (2013), 1714–1717.
65. 65 Horner, C., Parnell, P., Hall, D., Kearns, A., Heritage, J., Wilcox, M., Meticillin-resistant Staphylococcus aureus in elderly residents of care homes: colonization rates and molecular epidemiology. J Hosp Infect 83 (2013), 212–218.
66. 66 Petinaki, E., Spiliopoulou, I., Kontos, F., et al. Clonal dissemination of mupirocin-resistant staphylococci in Greek hospitals. J Antimicrob Chemother 53 (2004), 105–108.
67. 67 Ahmed, M.O., Elramalli, A.K., Amri, S.G., Abuzweda, A.R., Abouzeed, Y.M., Isolation and screening of methicillin-resistant Staphylococcus aureus from health care workers in Libyan hospitals. East Mediterr Health J 18 (2012), 37–42.
68. 68 Poovelikunnel, T., Gethin, G., Humphreys, H., Mupirocin resistance: clinical implications and potential alternatives for the eradication of MRSA. J Antimicrob Chemother 70 (2015), 2681–2692.
69. 69 Idelevich, E.A., von Eiff, C., Friedrich, A.W., et al. In vitro activity against Staphylococcus aureus of a novel antimicrobial agent, PRF-119, a recombinant chimeric bacteriophage endolysin. Antimicrob Agents Chemother 55 (2011), 4416–4419.
70. 70 von Eiff, C., Kokai-Kun, J.F., Becker, K., Peters, G., In vitro activity of recombinant lysostaphin against Staphylococcus aureus isolates from anterior nares and blood. Antimicrob Agents Chemother 47 (2003), 3613–3615.
71. 71 Steed, L.L., Costello, J., Lohia, S., Jones, T., Spannhake, E.W., Nguyen, S., Reduction of nasal Staphylococcus aureus carraige in health care professionals by treatment with a nonantibiotic, alcohol-based nasal antispetic. Am J Infect Control 42 (2014), 841–846.
72. 72 Liu, Q., Zhao, H., Han, L., Shu, W., Wu, Q., Ni, Y., Frequency of biocide-resistant genes and susceptibility to chlorhexidine in high-level mupirocin-resistant, methicillin-resistant Staphylococcus aureus (MuH MRSA). Diagn Microbiol Infect Dis 82 (2015), 278–283.
73. 73 Lepainteur, M., Royer, G., Bourrel, A.S., et al. Prevalence of resistance to antiseptics and mupirocin among invasive coagulase-negative staphylococci from very preterm neonates in NICU: the creeping threat?. J Hosp Infect 83 (2013), 333–336.
74. 74 Ghasemzadeh-Moghaddam, H., van Belkum, A., Harmat, R.A., van Wamel, W., Neela, V., Methicillin-susceptible and -resistant Staphylococcus aureus with high-level antiseptic and low-level mupirocin resistance in Malaysia. Microb Drug Resist 20 (2014), 472–477.
75. 75 Trouillet-Assant, S., Flammier, S., Sapin, A., et al. Mupirocin resistance in isolates of Staphylococcus spp. from nasal swabs in a tertiary hospital in France. J Clin Microbiol 53 (2015), 2713–2715.
76. 76 Kaur, D.C., Chate, S.S., Study of antibiotic resistance pattern in methicillin-resistant Staphylococcus aureus with special reference to newer antibiotics. J Glob Infect Dis 7 (2015), 78–84.
77. 77 Biedenbach, D.J., Bouchillon, S.K., Johnson, S.A., Hoban, D.J., Hackel, M., Susceptibility of Staphylococcus aureus to topical agents in the United States: a sentinel study. Clin Ther 36 (2014), 953–960.
78. 78 Barros, E.M., Ceotto, H., Bastos, M.C., dos Santos, K.R., Giambiagi-deMarval, M., Staphylococcus haemolyticus as an important hospital pathogen and carrier of methicillin resistance genes. J Clin Microbiol 50 (2012), 166–168.
79. 79 Liu, Q.Z., Wu, Q., Zhang, Y.B., et al. Prevalence of clinical meticillin-resistant Staphylococcus aureus (MRSA) with high-level mupirocin resistance in Shanghai and Wenzhou, China. Int J Antimicrob Agents 35 (2010), 114–118.
80. 80 Kresken, M., Hafner, D., Schmitz, F.J., Wichelhaus, T.A., Resistenzsituation bei klinisch wichtigen Infektionserregern gegenüber Antibiotika in Deutschland und im mitteleuropäischen Raum. Bericht über die Ergebnisse einer multizentrischen Studie der Arbeitsgemeinschaft Empfindlichkeitsprüfungen & Resistenz der Paul-Ehrlich-Gesellschaft für Chemotherapie e.V. aus dem Jahre 2007. 2009, Antiinfectives Intelligence, Rheinbach.
81. 81 O'Shea, S., Cotter, L., Creagh, S., Lydon, S., Lucey, B., Mupirocin resistance among staphylococci: trends in the southern region of Ireland. J Antimicrob Chemother 64 (2009), 649–650.
82. 82 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, 6, 2006, 125.
83. 83 Köck, R., Becker, K., Cookson, B., et al. Systematic literature analysis and review of targeted preventive measures to limit healthcare-associated infections by methicillin-resistant Staphylococcus aureus. Eurosurveill 19 (2014), 23–49.
84. 84 Van Rijen, M., Bonten, M., Wenzel, R., Kluytmans, J., Mupirocin ointment for preventing Staphylococcus aureus infections in nasal carriers. Cochrane Database Syst Rev, 4, 2008, CD006216.
85. 85 Lee, A.S., Cooper, B., Malhotra-Kumar, S., et al. Comparison of strategies to reduce methicillin-resistant Staphylococcus aureus rates in surgical patients: a controlled multicentre interventional trial. Br Med J 3 (2013), 1–18.
86. 86 Schweizer, M.L., Chiang, H.-Y., Septimus, E., et al. Association of a bundled intervention with surgical site infections among patients undergoing cardiac, hip or knee surgery. JAMA 313 (2015), 2162–2171.
87. 87 Schelenz, S., Tucker, D., Georgeu, C., et al. Significant reduction of endemic MRSA acquisition and infection in cardiothoracic patients by means of an enhanced targeted infection control programme. J Hosp Infect 60 (2005), 104–110.
88. 88 Edmiston, C.E. Jr., Ledeboer, N.A., Buchan, B.W., Spencer, M., Seabrook, G.R., Leaper, D., Is staphylococcal screening and suppression an effective interventional strategy for reduction of surgical site infection?. Surg Infect 17 (2016), 1–9.
89. 89 Chen, A.F., Wessel, C.B., Rao, N., Staphylococcus aureus screening and decolonisation in orthopaedic surgery and reduction of surgical site infections. Clin Orthop Relat Res 471 (2013), 2383–2399.
90. 90 van Rijen, M.M., Bode, L.G., Baak, D.A., Kluytmans, J.A., Vos, M.C., Reduced costs for Staphylococcus aureus carriers treated prophylactically with mupirocin and chlorhexidine in cardiothoracic and orthopaedic surgery. PloS One, 7, 2012, e43065.
91. 91 Harbarth, S., Fankhauser, C., Schrenzel, J., et al. Universal screening for methicillin-resistant Staphylococcus aureus at hospital admission and nosocomial infection in surgical patients. JAMA 299 (2008), 1149–1157.
92. 92 Bode, L.G., Kluytmans, J.A., Wertheim, H.F., et al. Preventing surgical-site infections in nasal carriers of Staphylococcus aureus. N Engl J Med 362 (2010), 9–17.
93. 93 Bode, L.G., Rijen, M.M., Wertheim, H.F., et al. Long-term mortality after rapid screening and decolonization of Staphylococcus aureus carriers: observational follow-up study of a randomised, placebo-controlled trial. Ann Surg 263 (2016), 511–515.
94. 94 Spencer, M., Gulczynski, D., Stop SSIs in their track. OR Nurse 4 (2010), 38–42.
95. 95 Villamaria, F.C., Berlanga, G., Liao, I.C., et al. Comparison of environmental MRSA levels on high touch surfaces in contact isolation and noncontact isolation patient rooms. Infect Control Hosp Epidemiol 36 (2015), 1472–1475.
96. 96 Hardy, K.J., Oppenheim, B.A., Gossain, S., Gao, F., Hawkey, P.M., A study of the relationship between environmental contamination with methicillin-resistant Staphylococcus aureus and patients’ acquisition of MRSA. Infect Control Hosp Epidemiol 27 (2006), 127–132.
97. 97 Courville, X.F., Tomek, I.V., Kirkland, K.B., Birhle, Kantor, S.R., Finlayson, S.R.G., Cost-effectiveness of preoperative nasal mupirocin treatment in preventing surgical site infection in patients undergoing total hip and knee arthroplasty: a cost-effectiveness analysis. Infect Control Hosp Epidemiol 33 (2012), 152–159.
98. 98 Wassenberg, M.W., de Wit, G.A., Bonten, M.J., Cost-effectiveness of preoperative screening and eradication of Staphylococcus aureus carriage. PLoS Med, 6, 2011, e14815.
99. 99 Lee, B.Y., Wiringa, A.E., Bailey, R.R., et al. Screening cardiac surgery patients for MRSA: an economic computer model. Am J Manag Care 16 (2013), e163–e173.
100. 100 Lee, B.Y., Tsui, B.Y., Bailey, R.R., et al. Should vascular surgery patients be screened pre-operatively for methicillin-resistant Staphylococcus aureus?. Infect Control Hosp Epidemiol 30 (2009), 1158–1165.
101. 101 Clancy, C.J., Bartsch, S.M., Nguyegn, M.H., Stuckey, D.R., Shields, R.K., Lee, B.Y., A computer simulation model of the cost-effectiveness of routine Staphylococcus aureus screening and decolonisation among lung and heart-lung transplant recipients. Eur J Clin Microbiol Infect Dis 33 (2014), 1053–1061.
102. 102 Huang, S.S., Septimus, E., Kleinman, K., et al. Targeted versus decolonization to prevent ICU infection. N Engl J Med 368 (2013), 2255–2265.
103. 103 Upton, A., Lang, S., Heffernan, H., Mupirocin and Staphyloccoccus aureus: a recent paradigm of emerging antibiotic resistance. J Antimicrob Chemother 51 (2003), 613–617.
104. 104 Harbarth, S., Dharan, S., Liassine, N., Herrault, P., Auckenthaler, R., Pittet, D., Randomized, placebo-controlled, double-blind trial to evaluate the efficacy of mupirocin for eradicating carriage of methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 43 (1999), 1412–1416.
105. 105 Robicsek, A., Beaumont, J.L., Thomson, R.B., Govindarajan, G., Peterson, L.R., Topical therapy for methicillin-resistant Staphylococcus aureus colonisation: impact on infection risk. Infect Control Hosp Epidemiol 30 (2009), 623–632.
106. 106 Vivoni, A.M., Santos, K.R., de-Oliveira, M.P., et al. Mupirocin for controlling methicilin-resistant Staphylococcus aureus: lessons from a decade of use at a university hospital. Infect Control Hosp Epidemiol 26 (2005), 662–667.
107. 107 Deeny, S.R., Worby, C.J., Tosas-Auget, O., et al. Impact of mupirocin resistance on the transmission and control of healthcare-associated MRSA. J Antimicrob Chemother 70 (2015), 3366–3378.