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Evaluation of patients' skin, environmental surfaces, and urinary catheters as sources for transmission of urinary pathogens
American Journal of Infection Control xxx (2014) 1-3
Contents lists available at ScienceDirect
American Journal of Infection Control
American Journal of Infection Control
journal homepage: www.ajicjournal.org
Brief report
Evaluation of patients’ skin, environmental surfaces, and urinary catheters as sources for transmission of urinary pathogens Kathleen A. Linder MD a, Michelle T. Hecker MD b, Sirisha Kundrapu MD c, Jennifer L. Cadnum BS c, Jackson S. Musuuza BS d, Ajay K. Sethi PhD d, Curtis J. Donskey MD e, * a
Department of Medicine, University Hospitals Case Medical Center, Cleveland, OH MetroHealth Medical Center, Cleveland, OH Research Service, Cleveland VA Medical Center, Cleveland, OH d Department of Population Health Sciences, University of Wisconsin School of Medicine and Public Health, Madison, WI e Geriatric Research, Education and Clinical Center, Cleveland Veterans Affairs Medical Center, Cleveland, OH b c
Key Words: Urinary tract infection Asymptomatic bacteriuria Contamination Gram-positive
In hospitalized patients with urinary tract infection or asymptomatic bacteriuria, urinary pathogens frequently contaminate skin, high-touch environmental surfaces, and urinary catheters. Contamination is more common in patients with a urinary catheter in place and with gram-positive pathogens. Patients’ skin and environmental surfaces may provide an important source for transmission of urinary pathogens. Copyright Ó 2014 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
Urinary tract infection (UTI) is the most common health caree associated infection in the United States, accounting for approximately one-third of these infections occurring in hospitals.1 Asymptomatic bacteriuria (ASB) is also very common in health care settings, particularly in elderly patients and patients with indwelling urinary catheters.2-4 It is likely that patients with UTI or ASB provide the major reservoir for transmission of urinary pathogens.5 Although urinary pathogens are known to frequently contaminate the perineum of patients with UTI,4 information on the frequency of contamination of commonly examined skin sites and high-touch environmental surfaces in patients with bacteriuria is limited. Here we tested the hypothesis that skin and environmental contamination with urinary pathogens is common in patients with UTI or ASB, and evaluated risk factors for skin and/or environmental contamination.
* Address correspondence to Curtis J. Donskey, MD, Geriatric Research, Education and Clinical Center, Cleveland Veterans Affairs Medical Center, 10701 East Blvd, Cleveland, OH 44106. E-mail address: [email protected] (C.J. Donskey). This work was supported by the Department of Veterans Affairs, United States Government and by the Centers for Disease Control and Prevention (Grant R01 C100614-02, to C.J.D.). Conflict of interest: C.J.D has received research grants from STERIS, Pfizer, and GOJO, and has served on scientific advisory boards for 3M, EcoLab, and GOJO. There are no other conflicts of interest to report.
METHODS The Cleveland VA Medical Center Institutional Review Board approved the study protocol. During a 4-month period (July through October 2010), we conducted a prospective study of consecutive inpatients with bacteriuria (>105 colony-forming units of a urinary pathogen per mL of urine) identified in the microbiology laboratory. Medical records review was performed to obtain demographic data and information on medications, signs and symptoms of UTI, and laboratory tests. Patients were considered to have symptomatic UTI if urinary symptoms were documented (eg, dysuria, frequency, urgency, suprapubic or flank tenderness) and considered to have ASB if no symptoms were documented. Patients with indwelling urinary catheters and condom catheters were included in the analysis. Swabs were collected using BBL CultureSwabs (BD Diagnostic Systems, Sparks, MD) from standardized areas of each patient’s skin (combined arm and hand, combined chest and abdomen, axilla, and groin), environment (combined phone and call button and combined table and bed rail), and urinary catheter if present within 3 days of a positive urine culture. For skin and environmental sites, 5 10 cm areas were sampled, and for the hand, phone and call button, the entire surface area was sampled. For urinary catheters, the swab was applied to a 10-cm length of catheter at the exit site from the urethra.
0196-6553/$36.00 - Copyright Ó 2014 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ajic.2014.03.022
2
K.A. Linder et al. / American Journal of Infection Control xxx (2014) 1-3 Table 1 Characteristics of 54 study patients with a UTI or ASB, stratified by the presence or absence of skin and/or environmental contamination with the urinary pathogens
Characteristic
Fig 1. Frequency of contamination of skin and environmental sites in 54 patients with UTI or ASB, stratified by gram-positive (16 patients) and gram-negative (38 patients) urinary pathogens. Any environmental contamination does not include urinary catheter contamination. Skin or environmental contamination was considered present if pathogens concordant with the organism in urine were cultured.
Identification and susceptibility test results for urinary isolates were obtained from the microbiology laboratory. Based on these results, swabs were plated onto appropriate selective media agar to determine whether the urinary pathogen was present. Selective media included MacConkey agar for gram-negative bacilli, Enterococcosel agar for enterococci, and mannitol salt agar for staphylococci (all from BD Diagnostic Systems). After plating, the swabs were also incubated in 1 mL of brain-heart infusion broth (BD Diagnostic Systems) overnight and specimens with positive growth were plated onto appropriate selective media plates. Identification and susceptibility testing of isolates was performed in accordance with Clinical Laboratory Standards Institute guidelines.6 Skin, environment, and catheter isolates were considered to be concordant with the urinary isolates if identification and susceptibility results were identical. Bivariate analyses were conducted to compare characteristics of patients with versus without positive skin and/or environmental contamination; urinary catheter contamination was not included in these analyses. Fisher’s exact test was used for categorical data, and Student’s unpaired t test was used for normally distributed data. Data were analyzed using SPSS version 10.0 (SPSS, Chicago, IL) and Stata 11 (StataCorp, College Station, TX). RESULTS Of the 54 patients with bacteriuria enrolled in this study, 31 (57%) had skin and/or environmental contamination with pathogens concordant with the organism in urine, including 29 (54%) with skin contamination and 19 (35%) with contamination of 1 or more environmental sites. There was no difference in the frequency of skin and/or environmental contamination between patients with UTI (n ¼ 30) and those with ASB (n ¼ 24) (data not shown). Of the 31 patients with a urinary catheter (29 with an indwelling catheters and 2 with a condom catheter), 18 (82%) had contamination of the catheter; 17 of these 18 (94%) had contamination of skin or other environmental sites. Thirty-eight patients (70%) had gram-negative pathogens in urine, and 16 (30%) had gram-positive pathogens. The most common gram-negative pathogens in urine were Klebsiella pneumoniae (n ¼ 12), Proteus mirabilis (n ¼ 9), Escherichia coli (n ¼ 6), and Pseudomonas aeruginosa (n ¼ 5); the gram-positive pathogens were Enterococcus spp (n ¼ 13) and Staphylococcus aureus (n ¼ 3).
Skin/ No skin/ environmental environmental All subjects contamination contamination P (n ¼ 54) (n ¼ 31) (n ¼ 23) value
Age, y mean (SD) 68 (14) Length of stay, d, median 5.5 (2-29) (IQR) Urinary catheter, n (%) 31 Male sex, n (%) 49 Nursing home resident, 12 n (%) Antibiotic use in the past 40 month, n (%) Urinary incontinence, 7 n (%) Decreased mobility, 15 n (%)* Organism type, n (%) Gram-negative 38 Gram-positive 16 Dementia, n (%) 10
66 (16) 5 (2-28)
71 (11) 5 (2-40)
.13 .53
22 (71) 29 (94) 9 (29)
9 (39) 20 (87) 3 (13)
.03 .64 .20
22 (71)
18 (78)
.75
4 (13)
3 (13)
1.00
12 (39)
3 (13)
.06
17 (55) 14 (45) 4 (13)
21 (91) 2 (9) 6 (19)
.006 .29
IQR, interquartile range; SD, standard deviation. *Decreased mobility was defined as a score of 1 or 2 on the mobility subcategory of the Braden score for prediction of pressure ulcer risk (1, completely immobile; 2, very limited; 3, slightly limited; 4, no limitation).
Figure 1 shows the frequency of contamination of different skin and environmental sites for patients with bacteriuria with grampositive and gram-negative pathogens. Table 1 shows a comparison of the characteristics of 31 patients with and 23 patients without skin and/or environmental contamination. The presence of urinary catheter and gram-positive pathogens in urine was significantly associated with skin and/or environmental contamination. In addition, decreased mobility was more common in patients with skin and/or environmental contamination, but the difference was not statistically significant. There were no significant differences in any other characteristic, including age, sex, length of stay, ward, nursing home residence, previous surgical history, previous use of antibiotics, diarrhea, urinary or fecal incontinence, dementia, or cerebrovascular accident. DISCUSSION In our hospitalized patients with UTI or ASB, urinary pathogens frequently contaminated skin, high-touch environmental surfaces, and urinary catheters. Contamination was significantly more common in patients with urinary catheters and with gram-positive pathogens in urine, and there was a trend toward increased contamination in patients with decreased mobility. These findings provide support for the hypothesis that skin and environmental surfaces of patients with bacteriuria represent an important source for transmission of urinary pathogens. The finding that urinary catheters are associated with skin and environmental contamination with urinary pathogens is consistent with previous studies demonstrating an association between indwelling devices and skin and/or environmental contamination in patients colonized with methicillin-resistant S aureus.7,8 Urinary catheters might increase the risk for skin contamination with urinary pathogens due to contamination of the external surface of the catheter and due to reduced ability to bathe effectively. The presence of the catheter may also increase the risk of skin and environmental contamination due to increased frequency of interactions with healthcare workers. The high frequency of contamination of skin and environmental surfaces with enterococci and S aureus is consistent with previous
K.A. Linder et al. / American Journal of Infection Control xxx (2014) 1-3
studies.8,9 These pathogens have been shown to survive for prolonged periods on dry surfaces. Some gram-negative pathogens (eg, E coli) may be less frequently detected on hospital surfaces owing to rapid loss of viability with dessication.10 An exception is Acinetobacter spp, which does survive well on dry surfaces10; none of the urinary isolates in this study were Acinetobacter spp, however. Our study has some limitations. The number of patients studied was small, and the majority were elderly men. Additional studies are needed to confirm our findings in other patient populations. Molecular typing was not performed to definitively confirm that skin and environmental isolates matched concurrent urinary isolates; however, isolates were considered concordant only if identification and susceptibility results were identical. Finally, we did not culture the hands of health care workers to assess whether skin and environmental isolates were being transferred to hands. In summary, urinary pathogens frequently contaminated commonly examined skin sites, high-touch environmental surfaces, and urinary catheters of hospitalized patients with UTI or ASB. Education of health care workers on the risk for transmission of urinary pathogens after contact with these sites is needed. Future studies should examine whether interventions such as skin and environmental disinfection can reduce the risk for transmission from patients with bacteriuria.
3
References 1. Klevens RM, Edwards JR, Richards CL Jr, Horan JC, Gaines RP, Pollock DA, et al. Estimating health careeassociated infections and deaths in US hospitals, 2002. Public Health Rep 2007;122:160-6. 2. Nicolle LE, Bradley S, Colgan R, Rice JC, Schaeffer A, Hooton TM. Infectious Diseases Society of America guidelines for the diagnosis and treatment of asymptomatic bacteriuria in adults. Clin Infect Dis 2005;40:643-54. 3. Nicolle LE. Urinary tract infections in long-term-care facilities. Infect Control Hosp Epidemiol 2001;22:167-75. 4. Nicolle LE. Urinary tract infection in long-term-care facility residents. Clin Infect Dis 2000;31:757-61. 5. Maki DG, Tambyah PA. Engineering out the risk of infection with urinary catheters. Emerg Infect Dis 2001;7:1-5. 6. Clinical Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing. CLSI M100eS20. Wayne [PA]: Clinical Laboratory Standards Institute; 2010. 7. Mody L, Kauffman CA, Donabedian S, Zervos M, Bradley SF. Epidemiology of Staphylococcus aureus colonization in nursing home residents. Clin Infect Dis 2008;46:1368-73. 8. Chang S, Sethi AK, Eckstein BC, Stiefel U, Cadnum JL, Donskey CJ. Skin and environmental contamination with MRSA among carriers identified clinically versus through active surveillance. Clin Infect Dis 2009;48:1423-8. 9. Sethi AK, Al-Nassir W, Nerandzic MM, Donskey CJ. Skin and environmental contamination with vancomycin-resistant enterococci in patients being treated with oral metronidazole versus oral vancomycin for Clostridium difficilee associated disease. Infect Control Hosp Epidemiol 2009;30:13-7. 10. Hirai Y. Survival of bacteria under dry conditions; from a viewpoint of nosocomial infection. J Hosp Infect 1991;19:191-200.
Contents lists available at ScienceDirect
American Journal of Infection Control
American Journal of Infection Control
journal homepage: www.ajicjournal.org
Brief report
Evaluation of patients’ skin, environmental surfaces, and urinary catheters as sources for transmission of urinary pathogens Kathleen A. Linder MD a, Michelle T. Hecker MD b, Sirisha Kundrapu MD c, Jennifer L. Cadnum BS c, Jackson S. Musuuza BS d, Ajay K. Sethi PhD d, Curtis J. Donskey MD e, * a
Department of Medicine, University Hospitals Case Medical Center, Cleveland, OH MetroHealth Medical Center, Cleveland, OH Research Service, Cleveland VA Medical Center, Cleveland, OH d Department of Population Health Sciences, University of Wisconsin School of Medicine and Public Health, Madison, WI e Geriatric Research, Education and Clinical Center, Cleveland Veterans Affairs Medical Center, Cleveland, OH b c
Key Words: Urinary tract infection Asymptomatic bacteriuria Contamination Gram-positive
In hospitalized patients with urinary tract infection or asymptomatic bacteriuria, urinary pathogens frequently contaminate skin, high-touch environmental surfaces, and urinary catheters. Contamination is more common in patients with a urinary catheter in place and with gram-positive pathogens. Patients’ skin and environmental surfaces may provide an important source for transmission of urinary pathogens. Copyright Ó 2014 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
Urinary tract infection (UTI) is the most common health caree associated infection in the United States, accounting for approximately one-third of these infections occurring in hospitals.1 Asymptomatic bacteriuria (ASB) is also very common in health care settings, particularly in elderly patients and patients with indwelling urinary catheters.2-4 It is likely that patients with UTI or ASB provide the major reservoir for transmission of urinary pathogens.5 Although urinary pathogens are known to frequently contaminate the perineum of patients with UTI,4 information on the frequency of contamination of commonly examined skin sites and high-touch environmental surfaces in patients with bacteriuria is limited. Here we tested the hypothesis that skin and environmental contamination with urinary pathogens is common in patients with UTI or ASB, and evaluated risk factors for skin and/or environmental contamination.
* Address correspondence to Curtis J. Donskey, MD, Geriatric Research, Education and Clinical Center, Cleveland Veterans Affairs Medical Center, 10701 East Blvd, Cleveland, OH 44106. E-mail address: [email protected] (C.J. Donskey). This work was supported by the Department of Veterans Affairs, United States Government and by the Centers for Disease Control and Prevention (Grant R01 C100614-02, to C.J.D.). Conflict of interest: C.J.D has received research grants from STERIS, Pfizer, and GOJO, and has served on scientific advisory boards for 3M, EcoLab, and GOJO. There are no other conflicts of interest to report.
METHODS The Cleveland VA Medical Center Institutional Review Board approved the study protocol. During a 4-month period (July through October 2010), we conducted a prospective study of consecutive inpatients with bacteriuria (>105 colony-forming units of a urinary pathogen per mL of urine) identified in the microbiology laboratory. Medical records review was performed to obtain demographic data and information on medications, signs and symptoms of UTI, and laboratory tests. Patients were considered to have symptomatic UTI if urinary symptoms were documented (eg, dysuria, frequency, urgency, suprapubic or flank tenderness) and considered to have ASB if no symptoms were documented. Patients with indwelling urinary catheters and condom catheters were included in the analysis. Swabs were collected using BBL CultureSwabs (BD Diagnostic Systems, Sparks, MD) from standardized areas of each patient’s skin (combined arm and hand, combined chest and abdomen, axilla, and groin), environment (combined phone and call button and combined table and bed rail), and urinary catheter if present within 3 days of a positive urine culture. For skin and environmental sites, 5 10 cm areas were sampled, and for the hand, phone and call button, the entire surface area was sampled. For urinary catheters, the swab was applied to a 10-cm length of catheter at the exit site from the urethra.
0196-6553/$36.00 - Copyright Ó 2014 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ajic.2014.03.022
2
K.A. Linder et al. / American Journal of Infection Control xxx (2014) 1-3 Table 1 Characteristics of 54 study patients with a UTI or ASB, stratified by the presence or absence of skin and/or environmental contamination with the urinary pathogens
Characteristic
Fig 1. Frequency of contamination of skin and environmental sites in 54 patients with UTI or ASB, stratified by gram-positive (16 patients) and gram-negative (38 patients) urinary pathogens. Any environmental contamination does not include urinary catheter contamination. Skin or environmental contamination was considered present if pathogens concordant with the organism in urine were cultured.
Identification and susceptibility test results for urinary isolates were obtained from the microbiology laboratory. Based on these results, swabs were plated onto appropriate selective media agar to determine whether the urinary pathogen was present. Selective media included MacConkey agar for gram-negative bacilli, Enterococcosel agar for enterococci, and mannitol salt agar for staphylococci (all from BD Diagnostic Systems). After plating, the swabs were also incubated in 1 mL of brain-heart infusion broth (BD Diagnostic Systems) overnight and specimens with positive growth were plated onto appropriate selective media plates. Identification and susceptibility testing of isolates was performed in accordance with Clinical Laboratory Standards Institute guidelines.6 Skin, environment, and catheter isolates were considered to be concordant with the urinary isolates if identification and susceptibility results were identical. Bivariate analyses were conducted to compare characteristics of patients with versus without positive skin and/or environmental contamination; urinary catheter contamination was not included in these analyses. Fisher’s exact test was used for categorical data, and Student’s unpaired t test was used for normally distributed data. Data were analyzed using SPSS version 10.0 (SPSS, Chicago, IL) and Stata 11 (StataCorp, College Station, TX). RESULTS Of the 54 patients with bacteriuria enrolled in this study, 31 (57%) had skin and/or environmental contamination with pathogens concordant with the organism in urine, including 29 (54%) with skin contamination and 19 (35%) with contamination of 1 or more environmental sites. There was no difference in the frequency of skin and/or environmental contamination between patients with UTI (n ¼ 30) and those with ASB (n ¼ 24) (data not shown). Of the 31 patients with a urinary catheter (29 with an indwelling catheters and 2 with a condom catheter), 18 (82%) had contamination of the catheter; 17 of these 18 (94%) had contamination of skin or other environmental sites. Thirty-eight patients (70%) had gram-negative pathogens in urine, and 16 (30%) had gram-positive pathogens. The most common gram-negative pathogens in urine were Klebsiella pneumoniae (n ¼ 12), Proteus mirabilis (n ¼ 9), Escherichia coli (n ¼ 6), and Pseudomonas aeruginosa (n ¼ 5); the gram-positive pathogens were Enterococcus spp (n ¼ 13) and Staphylococcus aureus (n ¼ 3).
Skin/ No skin/ environmental environmental All subjects contamination contamination P (n ¼ 54) (n ¼ 31) (n ¼ 23) value
Age, y mean (SD) 68 (14) Length of stay, d, median 5.5 (2-29) (IQR) Urinary catheter, n (%) 31 Male sex, n (%) 49 Nursing home resident, 12 n (%) Antibiotic use in the past 40 month, n (%) Urinary incontinence, 7 n (%) Decreased mobility, 15 n (%)* Organism type, n (%) Gram-negative 38 Gram-positive 16 Dementia, n (%) 10
66 (16) 5 (2-28)
71 (11) 5 (2-40)
.13 .53
22 (71) 29 (94) 9 (29)
9 (39) 20 (87) 3 (13)
.03 .64 .20
22 (71)
18 (78)
.75
4 (13)
3 (13)
1.00
12 (39)
3 (13)
.06
17 (55) 14 (45) 4 (13)
21 (91) 2 (9) 6 (19)
.006 .29
IQR, interquartile range; SD, standard deviation. *Decreased mobility was defined as a score of 1 or 2 on the mobility subcategory of the Braden score for prediction of pressure ulcer risk (1, completely immobile; 2, very limited; 3, slightly limited; 4, no limitation).
Figure 1 shows the frequency of contamination of different skin and environmental sites for patients with bacteriuria with grampositive and gram-negative pathogens. Table 1 shows a comparison of the characteristics of 31 patients with and 23 patients without skin and/or environmental contamination. The presence of urinary catheter and gram-positive pathogens in urine was significantly associated with skin and/or environmental contamination. In addition, decreased mobility was more common in patients with skin and/or environmental contamination, but the difference was not statistically significant. There were no significant differences in any other characteristic, including age, sex, length of stay, ward, nursing home residence, previous surgical history, previous use of antibiotics, diarrhea, urinary or fecal incontinence, dementia, or cerebrovascular accident. DISCUSSION In our hospitalized patients with UTI or ASB, urinary pathogens frequently contaminated skin, high-touch environmental surfaces, and urinary catheters. Contamination was significantly more common in patients with urinary catheters and with gram-positive pathogens in urine, and there was a trend toward increased contamination in patients with decreased mobility. These findings provide support for the hypothesis that skin and environmental surfaces of patients with bacteriuria represent an important source for transmission of urinary pathogens. The finding that urinary catheters are associated with skin and environmental contamination with urinary pathogens is consistent with previous studies demonstrating an association between indwelling devices and skin and/or environmental contamination in patients colonized with methicillin-resistant S aureus.7,8 Urinary catheters might increase the risk for skin contamination with urinary pathogens due to contamination of the external surface of the catheter and due to reduced ability to bathe effectively. The presence of the catheter may also increase the risk of skin and environmental contamination due to increased frequency of interactions with healthcare workers. The high frequency of contamination of skin and environmental surfaces with enterococci and S aureus is consistent with previous
K.A. Linder et al. / American Journal of Infection Control xxx (2014) 1-3
studies.8,9 These pathogens have been shown to survive for prolonged periods on dry surfaces. Some gram-negative pathogens (eg, E coli) may be less frequently detected on hospital surfaces owing to rapid loss of viability with dessication.10 An exception is Acinetobacter spp, which does survive well on dry surfaces10; none of the urinary isolates in this study were Acinetobacter spp, however. Our study has some limitations. The number of patients studied was small, and the majority were elderly men. Additional studies are needed to confirm our findings in other patient populations. Molecular typing was not performed to definitively confirm that skin and environmental isolates matched concurrent urinary isolates; however, isolates were considered concordant only if identification and susceptibility results were identical. Finally, we did not culture the hands of health care workers to assess whether skin and environmental isolates were being transferred to hands. In summary, urinary pathogens frequently contaminated commonly examined skin sites, high-touch environmental surfaces, and urinary catheters of hospitalized patients with UTI or ASB. Education of health care workers on the risk for transmission of urinary pathogens after contact with these sites is needed. Future studies should examine whether interventions such as skin and environmental disinfection can reduce the risk for transmission from patients with bacteriuria.
3
References 1. Klevens RM, Edwards JR, Richards CL Jr, Horan JC, Gaines RP, Pollock DA, et al. Estimating health careeassociated infections and deaths in US hospitals, 2002. Public Health Rep 2007;122:160-6. 2. Nicolle LE, Bradley S, Colgan R, Rice JC, Schaeffer A, Hooton TM. Infectious Diseases Society of America guidelines for the diagnosis and treatment of asymptomatic bacteriuria in adults. Clin Infect Dis 2005;40:643-54. 3. Nicolle LE. Urinary tract infections in long-term-care facilities. Infect Control Hosp Epidemiol 2001;22:167-75. 4. Nicolle LE. Urinary tract infection in long-term-care facility residents. Clin Infect Dis 2000;31:757-61. 5. Maki DG, Tambyah PA. Engineering out the risk of infection with urinary catheters. Emerg Infect Dis 2001;7:1-5. 6. Clinical Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing. CLSI M100eS20. Wayne [PA]: Clinical Laboratory Standards Institute; 2010. 7. Mody L, Kauffman CA, Donabedian S, Zervos M, Bradley SF. Epidemiology of Staphylococcus aureus colonization in nursing home residents. Clin Infect Dis 2008;46:1368-73. 8. Chang S, Sethi AK, Eckstein BC, Stiefel U, Cadnum JL, Donskey CJ. Skin and environmental contamination with MRSA among carriers identified clinically versus through active surveillance. Clin Infect Dis 2009;48:1423-8. 9. Sethi AK, Al-Nassir W, Nerandzic MM, Donskey CJ. Skin and environmental contamination with vancomycin-resistant enterococci in patients being treated with oral metronidazole versus oral vancomycin for Clostridium difficilee associated disease. Infect Control Hosp Epidemiol 2009;30:13-7. 10. Hirai Y. Survival of bacteria under dry conditions; from a viewpoint of nosocomial infection. J Hosp Infect 1991;19:191-200.