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Methicillin-resistant Staphylococcus aureus (MRSA) in the institutionalized older patient

Published online by Cambridge University Press:  14 September 2009

M Eveillard*
Affiliation:
Laboratoire de Bactériologie-hygiène, Centre Hospitalier Universitaire, Angers, France
ML Joly-Guillou
Affiliation:
Laboratoire de Bactériologie-hygiène, Centre Hospitalier Universitaire, Angers, France
*
Address for correspondence: M Eveillard, Laboratoire de Bactériologie-hygiène, CHU Angers, 4 rue Larrey, F-49000, France. Email: [email protected]

Summary

Nursing homes and long-term care facilities are usually considered as reservoirs for methicillin-resistant Staphylococcus aureus (MRSA) carriers. Actually, there are major differences in MRSA carriage between institutions, with variations from 1% to more than 30%. Overall there is a low incidence of MRSA infection in these institutions, even though carriage is associated with a higher risk of subsequent MRSA infection, with high mortality rates. The main risk factors for carriage are well known: recent hospitalization in an acute-care ward, skin wounds and recent antimicrobial therapy. Age over 75 years is also a risk factor. Residents of nursing homes and long-term care facilities pose a risk of MRSA transfer to acute-care wards, with potential consequences in terms of infection control strategy or surgical antibiotic prophylaxis. No well-designed study has identified the best strategy for MRSA control in institutions for older people and strategies that have been proposed are controversial. Studies to elucidate this would be useful, as well as studies specifically designed to identify the relative importance of different ways of MRSA transmission in these institutions (cross-transmission via healthcare workers or the environment, or direct transmission from one resident to another). Finally, a first important step towards MRSA control is a strict application of standard precautions, particularly good compliance with hand hygiene.

Type
Clinical geriatrics
Copyright
Copyright © Cambridge University Press 2009

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References

1Bonono, RA. Multiple antibiotic-resistant bacteria in long-term care facilities: an emerging problem in the practice of infectious diseases. Clin Infect Dis 2000; 31: 1414–22.CrossRefGoogle Scholar
2Garibaldi, RA. Residential care and the elderly: the burden of infection. J Hosp Infect 1999; 43 suppl: S918.CrossRefGoogle ScholarPubMed
3Alvarez, S, Shell, CG, Wooley, TW, Berk, SL, Smith, JK. Nosocomial infections in long-term care facilities. J Gerontol 1988; 43: M917.CrossRefGoogle Scholar
4Norman, DC, Castle, SC, Cantrell, M. Infections in the nursing home. J Am Geriatr Soc 1987; 35: 796805.CrossRefGoogle ScholarPubMed
5Fluit, AC, Wielders, CL, Verhoef, J, Schmitz, FJ. Epidemiology and susceptibility of 3051 Staphylococcus isolates from 25 university hospitals participating in the European SENTRY study. J Clin Microbiol 2001; 39: 3727–32.CrossRefGoogle Scholar
6National Nosocomial Infections Surveillance (NNIS) System report: data summary from January 1992 through June 2002, issued August 2001. Am J Infect Control 2003; 31: 481–98.Google Scholar
7Strausbaugh, LJ, Jacobson, C, Sewell, DL, Potter, S, Ward, TT. Methicillin-resistant Staphylococcus aureus in extended care facilities: experiences in a Veteran's Affairs nursing home and a review of the literature. Infect Control Hosp Epidemiol 1992; 13: 711–8.CrossRefGoogle Scholar
8Baba, T, Takeuchi, F, Kuroda, M et al. Genome and virulence determinants of high-virulence community-acquired MRSA. Lancet 2002; 359: 1819–27.CrossRefGoogle ScholarPubMed
9Okuma, K, Iwakawa, K, Turnidge, JD et al. Dissemination of new methicillin-resistant Staphylococcus aureus clones in the community. J Clin Microbiol 2002; 40: 4289–94.CrossRefGoogle ScholarPubMed
10Vandenesch, F, Naimi, T, Enright, MC et al. Community-acquired methicillin-resistant Staphylococcus aureus carrying Panton-Valentine leukocidin genes: worldwide emergence. Emerg Infect Dis 2003; 9: 978–84.CrossRefGoogle ScholarPubMed
11Miller, G, Perdreau-Remington, F, Rieg, G et al. Necrotizing fasciitis caused by community-associated methicillin-resistant Staphylococcus aureus in Los Angeles. N Eng J Med 2005; 352: 1445–53.CrossRefGoogle ScholarPubMed
12Muto, CA, Jernigan, JA, Ostrowsky, BE et al. SHEA guideline for preventing nosocomial transmission of multidrug-resistant strains of Staphylocccus aureus and enterococcus. Infect Control Hosp Epidemiol 2003; 24: 362–86.CrossRefGoogle Scholar
13Hospital Infection Control Advisory Committee (HICPAC). Management of multidrug-resistant organisms in healthcare settings 2006. http://www.cdc.gov/ncidod/dhqp/pdf/ar/mdroGuideline2006.pdfGoogle Scholar
14Infection control strategies for preventing the transmission of methicillin-resistant Staphylococcus aureus (MRSA) in nursing homes for older people. Cochrane Database Syst Rev 2008; 23: CD006354.Google Scholar
15Bradley, SF. Issues in the management of resistant bacteria in long-term care facilities. Infect Control Hosp Epidemiol 1999; 20: 362–6.CrossRefGoogle ScholarPubMed
16Bradley, SF, Terpenning, MS, Ramsey, MA, Zarins, LT, Jorgensen, KA, Sottile, WS et al. Methicillin-resistant Staphylococcus aureus: colonisation and infection in a long-term care facility. Ann Intern Med 1991; 115: 417–22.CrossRefGoogle ScholarPubMed
17Baldwin, NS, Gilpin, DF, Hughes, CM, Kearney, MP, Cardwell, C, Tunney, MM. Prevalence of methicillin-resistant Staphylococcus aureus colonization in residents and staff in nursing homes in Northern Ireland. J Am Geriatr Soc 2009; 57: 620–6.CrossRefGoogle ScholarPubMed
18Eveillard, M, Martin, Y, Hidri, N, Boussougant, Y, Joly-Guillou, ML. Carriage of methicillin-resistant Staphylococcus aureus among hospital employees: prevalence, duration and transmission to households. Infect Control Hosp Epidemiol 2004; 25: 114–20.CrossRefGoogle ScholarPubMed
19Eveillard, M, Charru, P, Rufat, P et al. Methicillin-resistant Staphylococcus aureus carriage in a long-term care facility: hypothesis about selection and transmission. Age Ageing 2008; 37: 294–9.CrossRefGoogle Scholar
20Brugnaro, P, Fedeli, U, Pellizzer, G et al. Clustering and risk factors of methicillin-resistant Staphylococcus aureus carriage in two Italian long-term care facilities. Infection 2009; 37: 216–21.CrossRefGoogle ScholarPubMed
21Cretnik, TZ, Vovko, P, Retelj, M, Jutersek, B, Harlander, T, Kolman, J, Gubina, M. Prevalence and nosocomial spread of methicillin-resistant Staphylococcus aureus in a long-term-care facility in Slovenia. Infect Control Hosp Epidemiol 2005; 26: 184–90.CrossRefGoogle Scholar
22Manzur, A, Gavalda, L, Ruiz de Gopegui, E et al. Group of the Spanish Network for Research in Infectious Diseases. Prevalence of methicillin-resistant Staphylococcus aureus and factors associated with colonization among residents in community long-term care facilities in Spain. Clin Microbiol Infect 2008; 14: 867–72.CrossRefGoogle Scholar
23Barr, B, Wilcox, MH, Brady, A, Parnell, P, Darby, B, Tompkins, D. Prevalence of methicillin-resistant Staphylococcus aureus colonization among older residents of care homes in the United Kingdom. Infect Control Hosp Epidemiol 2007; 28: 853–9.CrossRefGoogle ScholarPubMed
24Stone, ND, Lewis, DR, Lowery, HK et al. Importance of bacterial burden among methicillin-resistant Staphylococcus aureus carriers in a long-term care facility. Infect Control Hosp Epidemiol 2008; 29: 143–8.CrossRefGoogle ScholarPubMed
25Pop-Vicas, A, Mitchell, SL, Kandel, R, Schreiber, R, D'agata, EM. Multidrug-resistant gram-negative bacteria in a long-term care facility: prevalence and risk factors. J Am Geriatr Soc 2008; 56: 1276–80.CrossRefGoogle Scholar
26von Baum, H, Svoboda, D, Bock-Hensley, O, Wendt, C. Risk factors for methicillin-resistant Staphylococcus aureus carriage in residents of German nursing homes. Infect Control Hosp Epidemiol 2002; 23: 511–5.CrossRefGoogle ScholarPubMed
27Mendelson, G, Yearmack, Y, Granot, E, Ben-Israel, J, Colodner, R, Raz, R. Staphylococcus aureus carrier state among elderly residents of a long-term care facility. J Am Med Dir Assoc 2003; 4: 125–7.CrossRefGoogle ScholarPubMed
28Sie, I, Thorstad, M, Andersen, BM. Infection control and methicillin-resistant Staphylococcus aureus in nursing homes in Oslo. J Hosp Infect 2008; 70: 235–40.CrossRefGoogle ScholarPubMed
29Kotilainen, P, Routamaa, M, Peltonen, R et al. Eradication of methicillin-resistant Staphylococcus aureus from health center ward and associated nursing home. Arch Intern Med 2001; 161: 859–63.CrossRefGoogle Scholar
30Wagenlehner, FME, Naber, KG, Bambl, E et al. Management of a large healthcare-associated outbreak of Panton-Valentine leucocidin-positive methicillin-resistant Staphylococcus aureus in Germany. J Hosp Infect 2007; 67: 114–20.CrossRefGoogle ScholarPubMed
31Maltezou, HC, Vourli, S, Katerelos, P et al. Panton-Valentine leucocidin-positive methicillin-resistant Staphylococcus aureus outbreak among healthcare workers in a long-term care facility. Int J Infect Dis 2009 (in press).CrossRefGoogle Scholar
32Smith, CS, Parnell, P, Hodgson, G et al. Are methicillin-resistant Staphylococcus aureus that produce Panton-Valentine leucocidin (PVL) found among residents of care homes? J Antimicrob Chemother 2008; 62: 968–72.CrossRefGoogle ScholarPubMed
33Vovko, P, Retelj, M, Cretnik, TZ et al. Risk factors for colonisation with MRSA in a LTCF in Slovenia. Infect Control Hosp Epidemiol 2005; 26: 191–5.CrossRefGoogle Scholar
34Mody, L, Maheshwari, S, Galecki, A, Kauffman, CA, Bradley, SF. Indwelling device use and antibiotic resistance in nursing homes: identifying a high-risk group. J Am Geriatr Soc 2007; 55: 1921–6.CrossRefGoogle ScholarPubMed
35O'Sullivan, NP, Keane, CT. Risk factors for colonization with methicillin-resistant Staphylococcus aureus among nursing home residents. J Hosp Infect 2000; 45: 206–10.CrossRefGoogle ScholarPubMed
36Suetens, C, Niclaes, L, Jans, B et al. Determinants of methicillin-resistant Staphylococcus aureus carriage in nursing homes. Age Ageing 2007; 36: 327–30.CrossRefGoogle ScholarPubMed
37Pickering, TD, Gurwitz, JH, Zaleznik, D et al. The appropriateness of fluoroquinolone prescribing in the long-term setting. J Am Geriatr Soc 1994; 42: 2832.CrossRefGoogle Scholar
38Muller, A, Mauny, F, Talon, D et al. Effect of individual- and group-level antibiotic exposure on MRSA isolation: a multivariate analysis. J Antimicrob Chemother 2006; 58: 878–81.CrossRefGoogle Scholar
39Le Blanc, L, Pepin, J, Toulouse, K et al. Fluoroquinolones and risk of methicillin-resistant Staphylococcus aureus, Canada. Emerg Infect Dis 2006; 12: 13981405.CrossRefGoogle ScholarPubMed
40Cook, PP, Catrou, P, Gooch, M et al. Effect of reduction in ciprofloxacin use on prevalence of methicillin-resistant Staphylococcus aureus rates within individual units of a tertiary-care hospital. J Hosp Infect 2006; 64: 348–51.CrossRefGoogle ScholarPubMed
41Bello, TO, Taiwo, SS, Oparinde, DP et al. Risk of nosocomial bacteria transmission: evaluation of cleaning methods of probes used for routine ultrasonography. West Afr J Med 2005; 24: 167–70.CrossRefGoogle ScholarPubMed
42Eveillard, M, Mortier, E, Lancien, E et al. Consideration of age at admission for selective screening to identify methicillin-resistant Staphylococcus aureus carriers to control dissemination in a medical ward. Am J Infect Control 2006; 34: 108–13.CrossRefGoogle Scholar
43Buke, C, Armand-Lefevre, L, Lolom, I et al. Epidemiology of multidrug-resistant bacteria in patients with long hospital stays. Infect Control Hosp Epidemiol 2007; 28: 1255–60.CrossRefGoogle ScholarPubMed
44Eveillard, M, Ernst, C, Cuviller, S et al. Prevalence of methicillin-resistant Staphylococcus aureus carriage at the time of admission in two acute geriatric wards. J Hosp Infect 2002; 50: 122–6.CrossRefGoogle ScholarPubMed
45Lucet, JC, Grenet, K, Armand-Lefevre, L et al. High prevalence of methicillin-resistant Staphylococcus aureus at hospital admission in elderly patients: implications for infection control strategies. Infect Control Hosp Epidemiol 2005; 26: 121–6.CrossRefGoogle ScholarPubMed
46Merrer, J, Pisica-Donose, G, Neneveu, M, Pauthier, F. Prevalence of methicillin-resistant Staphylococcus aureus nasal carriage among patients with femoral neck fractures: implications for antibiotic prophylaxis. Infect Control Hosp Epidemiol 2004; 25: 515–7.CrossRefGoogle ScholarPubMed
47Manzur, A, Vidal, M, Pujol, M et al. Predictive factors of methicillin resistance among patients with Staphylococcus aureus bloodstream infections at hospital admission. J Hosp Infect 2007; 66: 135–41.CrossRefGoogle ScholarPubMed
48Eveillard, M, Leroy, C, Teissiere, F et al. Impact of selective screening in the emergency department on methicillin-resistant Staphylococcus aureus control programmes. J Hosp Infect 2006; 63: 380–4.CrossRefGoogle ScholarPubMed
49Muder, RR, Brennen, C, Wagener, MM et al. Methicillin-resistant staphylococcal colonization and infection in a long-term care facility. Ann Intern Med 1991; 114: 107–12.CrossRefGoogle ScholarPubMed
50Lee, YL, Cesario, T, Gupta, G et al. Surveillance of colonization and infection with Staphylococcus aureus susceptible or resistant to methicillin in a community skilled-nursing facility. Am J Infect Control 1997; 25: 312–21.CrossRefGoogle ScholarPubMed
51Mulhausen, PL, Harrel, LJ, Weinberger, M, Kochersberger, GG, Feussner, JR. Contrasting methicillin-resistant Staphylococcus aureus colonisation in Veterans Affairs and community nursing homes. Am J Med 1996; 100: 2431.CrossRefGoogle ScholarPubMed
52Safdar, N, Bradley, EA. The risk of infection after nasal colonization with Staphylococcus aureus. Am J Med 2008; 121: 310–5.CrossRefGoogle ScholarPubMed
53Roghmann, MC. Predicting methicillin resistance and the effect of inadequate empiric therapy on survival in patients with Staphylococcus aureus bacteremia. Arch Intern Med 2000; 160: 1001–4.CrossRefGoogle Scholar
54Rezende, NA, Blumberg, HM, Metzger, BS, Larsen, NM, Ray, SM, McGowan, JE Jr.Risk factors for methicillin resistance among patients with Staphylococcus aureus bacteremia at the time of hospital admission. Am J Med Sci 2002; 323: 117–23.CrossRefGoogle ScholarPubMed
55Lodise, TP Jr, McKinnon, PS, Rybak, M. Prediction model to identify patients with Staphylococcus aureus bacteremia at risk for methicillin resistance. Infect Control Hosp Epidemiol 2003; 24: 655–61.CrossRefGoogle ScholarPubMed
56Johnson, LB, Bhan, A, Pawlak, J, Manzor, O, Saravolatz, LD. Changing epidemiology of community-onset methicillin-resistant Staphylococcus aureus bacteremia. Infect Control Hosp Epidemiol 2003; 24: 431–5.CrossRefGoogle ScholarPubMed
57Lesse, AJ, Mylotte, JM. Clinical and molecular epidemiology of nursing home-associated Staphylococcus aureus bacteremia. Am J Infect Control 2006; 34: 642–50.CrossRefGoogle ScholarPubMed
58Hiramatsu, K, Aritaka, N, Hanaki, H et al. Dissemination in Japanese hospitals of strains of Staphylococcus aureus heterogeneously resistant to vancomycin. Lancet 1997; 350: 1670–3.CrossRefGoogle ScholarPubMed
59Appelbaum, PC. MRSA – the tip of the iceberg. Clin Microbiol Infect 2006; 12 (suppl 2): 310.CrossRefGoogle ScholarPubMed
60Tiwari, HK, Sen, MR. Emergence of vancomycin resistant Staphylococcus aureus (VRSA) from a tertiary care hospital from northern part of India. BMC Infect Dis 2006; 6: 156.CrossRefGoogle ScholarPubMed
61Appelbaum, PC. Reduced glycopeptide susceptibility in methicillin-resistant Staphylococcus aureus (MRSA). Int J Antimicrob Agents 2007; 30: 398408.CrossRefGoogle ScholarPubMed
62Niclaes, L, Buntinx, F, Bunaro, F, Lesaffre, E, Heyrman, J. Consequences of MRSA carriage in nursing homes residents. Epidemiol Infect 1999; 122: 235–9.CrossRefGoogle Scholar
63Lesens, O, Methlin, C, Hansmann, Y et al. Role of comorbidity in mortality related to Staphylococcus aureus bacteremia: a prospective study using the Charlson weighted index of comorbidity. Infect Control Hosp Epidemiol 2003; 24: 890–6.CrossRefGoogle ScholarPubMed
64Mylotte, JM, Tayara, A. Staphylococcus aureus bacteremia: predictors of 30-day mortality in a large cohort. Clin Infect Dis 2003; 31: 1170–4.CrossRefGoogle Scholar
65McClelland, RS, Fowler, VG Jr, Sanders, LL et al. Staphylococcus aureus bacteremia among elderly vs. younger adults patients: comparison of clinical features and mortality. Arch Intern Med 1999; 159: 1244–7.CrossRefGoogle ScholarPubMed
66Jensen, AG, Wachmann, CH, Espersen, F, Scheibel, J, Skinhoj, P, Frimodt-Moller, N. Treatment and outcome of Staphylococcus aureus bacteremia: a prospective study of 278 cases. Arch Intern Med 2002; 162: 2532.CrossRefGoogle ScholarPubMed
67Cosgrove, SE, Sakoulas, G, Perencevich, EN, Schwaber, MJ, Karchmer, AW, Carmeli, Y. Comparison of mortality associated with methicillin-resistant and methicillin-susceptible Staphylococcus aureus bacteremia: a meta-analysis. Clin Infect Dis 2003; 36: 53–9.CrossRefGoogle ScholarPubMed
68Sanford, MD, Widmer, AF, Bale, MJ, Jones, RN, Wenzel, RP. Efficient detection and long-term persistence of the carriage of methicillin-resistant Staphylococcus aureus. Clin Infect Dis 1994; 19: 1123–8.CrossRefGoogle ScholarPubMed
69Fraise, AP, Mitchell, K, O'Brien, SJ, Oldfield, K, Wise, R. Methicillin-resistant Staphylococcus aureus (MRSA) in nursing homes in a major UK city: an anonymized point prevalence survey. Epidemiol Infect 1997; 118: 15.CrossRefGoogle Scholar
70Hsu, CCS. Serial survey of methicillin-resistant Staphylococcus aureus nasal carriage among residents in a nursing home. Infect Control Hosp Epidemiol 1991; 12: 416–21.CrossRefGoogle ScholarPubMed
71Pittet, D, Allegranzi, B, Sax, H et al. Evidence-based model for hand transmission during patient care and the role of improved practices. Lancet Infect Dis 2006; 6: 641–52.CrossRefGoogle ScholarPubMed
72Dancer, SJ. Importance of the environment in methicillin-resistant Staphylococcus aureus acquisition: the case for hospital cleaning. Lancet Infect Dis 2008; 8: 101–13.CrossRefGoogle ScholarPubMed
73Dancer, SJ, White, L, Robertson, C. Monitoring environmental cleanliness on two surgical wards. Int J Environ Health Res 2008; 18: 357–64.CrossRefGoogle ScholarPubMed
74Dancer, SJ, White, LF, Lamb, J, Girvan, EK, Robertson, C. Measuring the effect of enhanced cleaning in a UK hospital: a prospective cross-over study. BMC Med 2009; 7: 28.CrossRefGoogle Scholar
75Trick, WE, Weinstein, RA, DeMarais, PL et al. Colonization of skilled-care facility residents with antimicrobial-resistant pathogens. J Am Geriatr Soc 2001; 49: 270–6.CrossRefGoogle ScholarPubMed
76O'Fallon, E, Gautam, S, D'Agata, EM. Colonisation with multidrug-resistant gram-negative bacteria: prolonged duration and frequent colonisation. Clin Infect Dis 2009; 48: 1375–81.CrossRefGoogle Scholar
77O'Fallon, E, Pop-Vicas, A, D'agata, E. The emerging threat of multidrug-resistant gram-negative organisms in long-term care facilities. J Gerontol A Biol Sci Med Sci 2009; 64: 138–41.CrossRefGoogle ScholarPubMed
78Minary-Dohen, P, Bailly, P, Bertrand, X, Talon, D. Methicillin-resistant Staphylococcus aureus (MRSA) in rehabilitation and chronic-care facilities: what is the best strategy? BMC Geriatr 2003; 3: 5.CrossRefGoogle ScholarPubMed
79Kreman, T, Hu, J, Pottinger, J, Herwaldt, LA. Survey of long-term-care facilities in Iowa for policies and practices regarding residents with methicillin-resistant Staphylococcus aureus or vancomycin-resistant enterococci. Infect Control Hosp Epidemiol 2005; 26: 811–5.CrossRefGoogle ScholarPubMed
80Larssen, KW, Jacobsen, T, Bergh, K, Tvete, P, Kvello, E, Scheel, O. Outbreak of methicillin-resistant Staphylococcus aureus in two nursing homes in Central Norway. J Hosp Infect 2005; 60: 312–6.CrossRefGoogle ScholarPubMed
81Lucet, JC, Chevret, S, Durand-Zaleski, I, Chastang, C, Régnier, B. Prevalence and risk factors for carriage of methicillin-resistant Staphylococcus aureus at admission to the intensive care unit. Arch Intern Med 2003; 163: 181–8.CrossRefGoogle ScholarPubMed
82Manian, FA, Senkel, D, Zack, J, Meyer, L. Routine screening for methicillin-resistant Staphylococcus aureus among patients newly admitted to an acute rehabilitation unit. Infect Control Hosp Epidemiol 2002; 23: 516–9.CrossRefGoogle Scholar
83Coello, R, Jiménez, J, Garcia, M et al. Prospective study of infection, colonization and carriage of methicillin-resistant Staphylococcus aureus in an outbreak affecting 990 patients. Eur J Clin Microbiol Infect Dis 1994; 13: 7481.CrossRefGoogle Scholar
84Eveillard, M, de Lassence, A, Lancien, E, Barnaud, G, Ricard, JD, Joly-Guillou, ML. Evaluation of a strategy of screening multiple anatomical sites for methicillin-resistant Staphylococcus aureus at admission to a teaching hospital. Infect Control Hosp Epidemiol 2002; 27: 181–4.CrossRefGoogle Scholar
85Batra, R, Eziefula, AC, Wyncoll, D, Edgeworth, J. Throat and rectal swabs may have an important role in MRSA screening for critically ill patients. Intensive Care Med 2008; 34: 1703–6.CrossRefGoogle ScholarPubMed
86Pan, A, Domenighini, F, Signorini, L et al. Adherence to hand hygiene in an Italian long-term care facility. Am J Infect Control 2008; 36: 495–7.CrossRefGoogle Scholar
87Huang, TT, Wu, SC. Evaluation of a training programme on knowledge and compliance of nurse assistants’ hand hygiene in nursing homes. J Hosp Infect 2008; 68: 164–70.CrossRefGoogle ScholarPubMed
88Eveillard, M, Hitoto, H, Raymond, F et al. Measurement and interpretation of hand hygiene compliance rates: importance of monitoring entire care episodes. J Hosp Infect 2009; 72: 211–7.CrossRefGoogle ScholarPubMed
89Haas, JP, Larson, EL. Measurement of compliance with hand hygiene. J Hosp Infect 2007; 66: 614.CrossRefGoogle ScholarPubMed
90Mody, L, McNeil, SA, Sun, R, Bradley, SE, Kauffman, CA. Introduction of a waterless alcohol-based hand rub in a long-term care facility. Infect Control Hosp Epidemiol 2003; 24: 165–71.CrossRefGoogle ScholarPubMed