Bacterial contamination of computer and hand hygiene compliance in the emergency department

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1 Hong Kong Journal of Emergency Medicine Bacterial contamination of computer and hand hygiene compliance in the emergency department DY Hong, SO Park, KR Lee, KJ Baek, HW Moon, SB Han, DH Shin Introduction: The aim of this study was to determine the degree and nature of bacterial contamination of computer equipment in three Korean emergency departments (ED). Methods: Hand hygiene practices of ED doctors and nurses were observed before contact with computer equipment. Microbiological swab samples were obtained from 112 multiple-user computer keyboards and electronic mice in the ED of three teaching hospitals. Isolated organisms were identified by a clinical microbiologist using Gram stain, colony morphology, and susceptibility test. Results: Of the 112 samples, 103 (92.0%) showed growth of organisms on culture. Thirty-eight (33.9%) pieces of computer equipment yielded multiple bacterial species. Coagulase-negative Staphylococcus was the most common microorganism isolated (85.7%). Methicillin-resistant Staphylococcus aureus was obtained from two keyboards in two hospitals (1.8%). Hand hygiene compliance was observed on 29.9% occasions. Hand hygiene compliance after patient contact (38.0%) was higher than after other environmental contact (20.7%). Conclusions: Multiple user computer equipment in the ED may serve as reservoirs for nosocomial infection. Hand hygiene should be performed before and after using all ED equipment, including computer equipment. (Hong Kong j.emerg.med. 2012;19: ) ED ED ED % % 85.7% 1.8% 29.9% Correspondence to: Park Sang O, MD Konkuk University Medical Center, Department of Emergency Medicine, Konkuk University School of Medicine, Neugdong-ro, Hwayang-dong, Gwangjin-gu, Seoul, Republic of Korea, kuhem.park@gmail.com Hong Dae Young, MD Lee Kyeong Ryong, MD Baek Kwang Je, MD Inha University Hospital, Department of Emergency Medicine, Sinheung-dong 3-ga, Jung-gu, Incheon, Republic of Korea, Han Seung Baik, MD Kangbuk Samsung Hospital, Department of Emergency Medicine, Sungkyunkwan University School of Medicine, Pyeong-dong, Jongno-gu, Seoul, Republic of Korea, Shin Dong Hyuk, MD Konkuk University Medical Center, Department of Laboratory Medicine, Konkuk University School of Medicine, Neugdong-ro, Hwayang-dong, Gwangjin-gu, Seoul, Republic of Korea, Moon Hee Won, MD

2 388 Hong Kong j. emerg. med. Vol. 19(6) Nov 2012 Keywords: Cross infection, handwashing, infection control 38.0% 20.7% ED ED Introduction Nosocomial infections are infections that develop within a health care facility or are produced by organisms acquired during a stay in a health care institution. These infections are an important cause of morbidity, mortality and increased medical costs in hospitals. Previous investigation has reported that nosocomial infections occur in 7-10% of hospitalised patients during their hospital stay. 1 Each year at least two million patients acquire nosocomial infections, resulting in deaths. The annual cost of treating nosocomial infections is estimated to be approximately $5 billion. 2 The most common mode of transmission of nosocomial pathogens is hand carriage by health care personnel. Several studies have evaluated the hospital environment as a vector for transmission of pathogens. These studies had demonstrated contamination of a variety of hospital environmental sources, including bronchoscopes, hospital pagers, tap handles, and Doppler probes. 3-7 While the role of the hospital environment as a reservoir of nosocomial pathogens is controversial, it may be involved in the transmission of nosocomial pathogens. Recently, computers have become more widely used in clinical areas and, as with many other devices, have the potential to act as reservoirs for the transmission of pathogens. This is, especially so as computer equipment such as keyboards and electronic mice have multiple users. Previous studies have examined bacterial contaminant of computer equipment in selected areas such as intensive care units (ICU) and operating theatres. 5,6,8 The emergency department (ED) has very large numbers of patients passing through it compared with these setting. We were not aware of any similar studies examining the rate of bacterial contamination of computer equipment in the ED. The aim of this study was to determine the degree and nature of bacterial contamination of multiple user computer equipment (computer keyboards and electronic mice) located in three EDs at urban teaching hospitals in Korea. We also aimed to determine the degree of health professional hand hygiene compliance with respect to patient care and computer usage. Methods Study design and setting This study was conducted in the EDs of three urban teaching hospitals in the Republic of Korea. The three hospitals involved were Konkuk University Medical Center, Seoul (hospital A), Inha University Hospital, Incheon (hospital B), and Kangbuk Samsung Hospital, Seoul (hospital C). The ED of hospitals A, B and C have approximately 50,000, 53,000, and 35,000 patients visit per year. The study was approved by the relevant human research and ethics committees of all participating hospitals. At the time of the study, a total of 112 computer items (56 keyboards and 56 electronic mice) were used for medical care in the three EDs. They were all conventional devices without plastic covers that had been in use for periods of one to five years. Although all the items were used frequently by doctors and nurses throughout the day for various aspects of medical care (order entry, access to laboratory test results, viewing of radiology findings, entry of patient data), none of the hospitals had a specific disinfection policy or periodic cleaning of these items. Monitoring hand hygiene compliance Each institution has its own hand hygiene strategy based on the World Health Organization (WHO) guidelines on hand hygiene in health care. 9 Before microbiological samples were taken, one of the authors observed the frequency of hand contact with computer

3 Hong et al./bacterial contamination of computer in ED 389 equipment and the associated hand hygiene compliance of doctors and nurses before contact with this equipment. The concept of "My five moments for hand hygiene" 10 has been described in relation to hand hygiene monitoring and this technique was used in this study. The observer introduced himself to the staff being observed and indicated unobtrusively the reason for his presence. He then, maintained a discreet presence to avoid interference. The observer made great effort to avoid excessive observation bias by not being too obvious, while not deceiving the observed doctors and nurses about the purpose of observation. Data collection on hand hygiene was collected over a 24 hour period in each of the three EDs. Staff were observed for a 20 minutes (min) period every four hours during this 24 hour period, resulting in six 20 min periods of observation of hand hygiene for each of the three hospitals. All opportunities for hand hygiene were classified according to the "Five moments" concept; before patient contact, before an aseptic/clean procedure, after body fluid exposure risk, after patient contact, and after contact with patient surroundings. We then dichotomised these "Five moments" as "patient contact" (before patient contact, after patient contact) and other environment contact (an aseptic/clean procedure, after body fluid exposure risk, contact with patient surroundings). Appropriate hand hygiene was defined as washing hands with water and soap or rubbing hands with an alcohol-containing preparation. Each hand hygiene opportunity just before computer equipment contact was then coded as to whether the individual complied or not. 9,10 In the same observational periods, the hand contacts with computer keyboards and electronic mice were observed. All observations were recorded manually on a preformatted data collection sheet in real time. Microbiological procedures Microbiological specimens were obtained from all the computer keyboards and electronic mice in the three EDs. The items of equipment sampled were located in various locations including resuscitation rooms, patient clinical areas, and central work-stations adjoining patient treatment areas. One of the authors took all the swabs in three EDs, wearing sterile gloves during the process. A single sterile swab moistened with a small amount of sterile saline was wiped over the keyboard and electronic mouse surfaces. Keyboards were sampled by moving the sterile swab over the all keys (letter keys, space bar, enter key, function keys, number keys and other keys) over 60 seconds. The areas tested on each mouse were the palm rest, left and right click buttons of the mouse, and a standard 6 cm 2 area was swabbed. Swabs were sent immediately to the clinical microbiology laboratory of hospital A. The specimens were inoculated onto trypticase soy agar with 5% sheep blood using a semi-quantitative method in which the swab was rolled across a blood agar plate several times. The specimens were incubated at 35 C for 48 h. The number of colonies growing on each plate was estimated daily after visible inspection by the clinical microbiologist of hospital A. Organisms isolated from positive cultures were identified using Gram's stain, and colony morphology and biochemical characteristics using the VITEK II Identification System (biomerieux, Marcy l'etoile, France). Susceptibility testing for oxacillin was performed on all Staphylococcus aureus (S. aureus) isolates by a disk diffusion method based on the Clinical and Laboratory Standards Institute guidelines. Statistical analysis A sample size was estimated using data from Hartmann et al in which there was a bacterial contaminutesation rate of approximately 85% in ICU computer equipment. 5 We estimated that the bacterial contamination rate of computer equipment in our ED to be approximately 80%. Using an alpha level of 0.05 and a power of 0.8, 97 samples would be required. Data were analysed using SPSS 12.0 for Windows. Associations of categorical variables were evaluated by chi-square test or Fisher's exact test. A P value of less than 0.05 was considered significant for all statistical comparisons. Results Bacterial contamination A total of 112 microbiological swabs were obtained

4 390 Hong Kong j. emerg. med. Vol. 19(6) Nov 2012 including 44 samples from hospital A (22 keyboards, 22 electronic mice), 42 samples from hospital B (21 keyboards, 21 electronic mice) and 26 samples (13 keyboards, 13 electronic mice) from hospital C. Of these 112 samples, 103 (92.0%) showed growth of organisms on culture, with 38 (33.9%) yielding multiple bacterial species. Coagulase-negative Staphylococcus (CNS) was the most common microorganism isolated (96/112 (85.7%)). Methicillinresistant S. aureus (MRSA) was obtained from two keyboards (one in each of two hospitals) (1.8%). Nine cultures showed no growth of microorganisms (8.0%). The rate of bacterial contamination was 98.2% for keyboards and 85.7% for electronic mice. Keyboards also showed a higher rate of contamination with multiple bacterial species [50.0% (95% CI 36%-64%) vs. 17.8% (95% CI 9%-30%)] (Table 1). Hand contacts and hand hygiene compliance Seventy-five doctors and nurses made contact with computer equipment during the observation period. In total, 2451 contacts with computer equipment were observed (1296 in keyboards and 1155 in electronic mice). On average, keyboards were contacted 8.3 times per hour and electronic mice 13.6 times per hour after contact with a patient or other environmental contact. Overall, hand hygiene compliance before contact with computer equipment was observed on 29.9% occasions. Hand hygiene compliance after patient contact was higher than after other environmental contact for both keyboards 42.2% (95% CI 38%-47%) vs. 23.4% (95% CI 19%-28%) and electronic mice 35.3% (95% CI 32%-39%) vs. 19.2% (95% CI 16%- 22%). Hand hygiene compliance was higher for keyboard use than for electronic mice after both patient contact and environmental contact (Table 2). Table 1. Numbers of computer keyboards and electronic mice contaminated and the organisms isolated Growth Total (n=112) Computer equipment P value Keyboards (n=56) Electronic mice (n=56) CNS Bacillus spp Gram-negative rods Micrococcus Moulds MRSA MSSA Multiple growth <0.001 No growth CNS=coagulase-negative Staphylococcus; MRSA=methicillin-resistant Staphylococcus aureus; MSSA=methicillin-sensitive S. aureus Table 2. Frequency of hand contact and hand hygiene compliance After patient contact After other contact P value Total Total contacts Contacts/hour* Perform hand hygiene 493 (38.0%, 95% CI 35-40) 239 (20.7%, 95% CI 18-23) <0.001 Keyboards Total contacts Contacts/hour* Perform hand hygiene 219 (42.2%, 95% CI 38-47) 96 (23.4%, 95% CI 19-28) <0.001 Mice Total contacts Contacts/hour* Perform hand hygiene 247 (35.3%, 95% CI 32-39) 143 (19.2%, 95% CI 16-22) <0.001 * Number of hand contacts with one keyboard or one mouse during one hour.

5 Hong et al./bacterial contamination of computer in ED 391 Discussion Previous studies have demonstrated that the hospital environment may act as a source of transmission of microorganisms associated with nosocomial infections. Oie et al found S. aureus contamination on 27% of hospital door handles with MRSA accounting for 8.7% of these. 11 Antibiotic-resistant bacteria have been shown to contaminate a variety of hospital objects, including blood pressure cuffs, bed rails, monitor dials, and Doppler probes Computer equipment has become an essential part of patient care in all areas of the hospital. Consequently, computer equipment may act as a reservoir for microorganisms and contribute to the transfer of potentially pathogenic bacteria to patients. Direct contact by doctors and nurses with patients and bedside computer equipment may put patients at risk. Immunocompromised or immunosuppressed patients who are more susceptible to infections may even die as a result of nosocomial infection. The study by Bures et al revealed a twofold higher contamination rate for computer keyboards (24%) than for tap handles (11%) in an ICU setting, and suggested that more frequent hand contact may explain the higher contamination rate of computer keyboards and electronic mice than of infusion pumps and ventilators. 6 In another study, 95% of the cultures from computer keyboards in acute care wards were positive for microorganisms. 16 In this study, we found that 92% of the cultures from computer keyboards and electronic mice were positive for microorganisms. Although most of these microorganisms were traditional skin flora, four keyboards were positive for pathogens such as S. aureus, known to be associated with nosocomial transmission. MRSA was isolated from only two computer keyboards, but MRSA was not found on any electronic mice. Previous study also had failed to demonstrate the presence of MRSA on computer electronic mice in the ED. 17 But, another study demonstrated that ambulance bay security keypad became contaminated with MRSA. 18 No studies have reliably demonstrated the lifespan of MRSA on inanimate objects in the ED. However, keyboards are used frequently by many different doctors and nurses (8.3 times per hour) greatly increasing the chances of spreading MRSA from this reservoir. Practices such as hand washing and barrier protection are considered the simplest and most important measures to prevent nosocomial infections in the hospital setting. Hand washing has been shown to reduce transmission of potential nosocomial pathogens and has also been reported to reduce mortality related to nosocomial infections. 19,20 The risk of carriage of potential nosocomial pathogens from bacterially contaminated computer keyboards and electronic mice would be reduced if health care personnel washed their hands before and after contact with patients. However, studies have documented poor compliance with this procedure in most hospitals. The rate of hand hygiene compliance reported in the literature ranges from 5-81% (overall average 40%). 21 In this study, we found that the rate of hand hygiene compliance before contact with computer equipment was very low in this emergency department setting (29.9%). There were also large differences in the hand hygiene compliance rate of health care personnel after patient contact and after contact with other environmental objects: after contact with an environmental object the median compliance was 20.7%, whereas after patient contact the median compliance was 38.0%. A recent study showed that the hand hygiene compliance rate of emergency department staff was much lower than other units (ED 19.2%, infectious disease unit 44.9%, ophthalmology unit 56.5%). 22 Although ultraviolet light disinfection reduced bacterial contamination on keyboards, but another study showed that ultraviolet light source alone was not sufficient to decontaminate computer keyboards. 23,24 Use of plastic keyboard and mouse covers combined with regular cleaning with disinfectants (alcohol, chlorine, phenol, etc.) may reduce bacterial contamination, but these do not provide protection against bacterial transmission. Frequent use by health care personnel leads to rapid recontamination of computer keyboards In addition, the effectiveness of routine surface disinfection measures in reducing nosocomial infection has not been clearly demonstrated. At such, a policy of strict-hand hygiene remains the mainstay of any measures to reduce nosocomial infections.

6 392 Hong Kong j. emerg. med. Vol. 19(6) Nov 2012 There were several limitations to this study. First, specimens were collected at random times. Variation in the frequency of hand contact and the last user of computer equipment may have lead to different outcomes. Second, direct observation could change hand hygiene compliance of staffs when they know that they are being observed. These modified their behaviour accordingly (the so-called "Hawthorne effect") cannot be evaluated in this study. A third limitation is that we focused only on one moment of hand hygiene (just prior to use of computer equipment) rather than the "Five Moments" of hand hygiene previously described. Furthermore, we did not take into consideration the duration of contact with computer items. Regardless of whether the item was used for a long time or a short time, all contact was recorded 'one contact'. Also, we did not record whether computer items were contacted more frequently than other hospital items. Conclusion We have demonstrated that bacterial contamination of multiple user computer equipment in the ED may be a source of nosocomial infection. MRSA could be isolated from only two keyboards, but these items are used frequently by multiple use. In an effort to prevent nosocomial infection, health care personnel should remember to wash their hands before patient contact (after using computer equipment) as well as after patient contact (before using the computer equipment). The potential benefit of these measures in the reduction of nosocomial infections remains to be studied. Acknowledgement This work was supported by Konkuk University in References 1. Smith RL 2nd, Sawyer RG, Pruett TL. Hospitalacquired infections in the surgical intensive care: epidemiology and prevention. Zentralbl Chir 2003;128 (12): Burke JP. Infection control- a problem for patient safety. N Engl J Med 2003;348(7): Sorin M, Segal-Maurer S, Mariano N, Urban C, Combest A, Rahal JJ. Nosocomial transmission of imipenem-resistant Pseudomonas aeruginosa following bronchoscopy associated with improper connection to the Steris System 1 processor. Infect Control Hosp Epidemiol 2001;22(7): Singh D, Kaur H, Gardner WG, Treen LB. Bacterial contamination of hospital pagers. Infect Control Hosp Epidemiol 2002;23: Hartmann B, Benson M, Junger A, Quinzio L, Röhrig R, Fengler B, et al. Computer keyboard and mouse as a reservoir of pathogens in an intensive care unit. J Clin Monit Comput 2004;18(1): Bures S, Fishbain JT, Uyehara CF, Parker JM, Berg BW. Computer keyboards and faucet handles as reservoirs of nosocomial pathogens in the intensive care unit. Am J Infect Control 2000;28(6): Kibria SM, Kerr KG, Dave J, Gough MJ, Homer- Vanniasinkam S, Mavor AI. Bacterial colonization of Doppler probes on vascular surgical wards. Eur J Vasc Endovasc Surg 2002;23(3); Fukada T, Iwakiri H, Ozaki M. Anaesthetists' role in computer keyboard contamination in an operating room. J Hosp Infect 2008;70(2): Pittet D, Allegranzi B, Boyce J; World Health Organization World Alliance for Patient Safety First Global Patient Safety Challenge Core Group of Experts. The World Health Organization Guidelines on Hand Hygiene in Health Care and their consensus recommendations. Infect Control Hosp Epidemiol 2009;30(7): Sax H, Allegranzi B, Chraïti MN, Boyce J, Larson E, Pittet D. The World Health Organization hand hygiene observation method. Am J Infect Control 2009;37(10): Oie S, Hosokawa I, Kamiya A. Contamination of room door handles by methicillin-sensitive/methicillinresistant Staphylococcus aureus. J Hosp Infect 2002; 51(2): Hayden MK, Blom DW, Lyle EA, Moore CG, Weinstein RA. Risk of hand or glove contamination after contact with patients colonized with vancomycinresistant enterococcus or the colonized patients' environment. Infect Control Hosp Epidemiol 2008;29 (2): Aygün G, Demirkiran O, Utku T, Mete B, Urkmez S, Yilmaz M, et al. Environmental contamination during a carbapenem-resistant Acinetobacter baumannii outbreak in an intensive care unit. J Hosp Infect 2002; 52(4): Whitehead EJ, Thompson JF, Lewis DR. Contamination and decontamination of Doppler probes. Ann R Coll Surg Engl 2006;88(5): Karadenz YM, Kiliç D, Kara Altan S, Altinok D, Güney S. Evaluation of the role of ultrasound machines as a source of nosocomial and cross-infection. Invest Radiol 2001;36(9):554-8.

7 Hong et al./bacterial contamination of computer in ED Schultz M, Gill J, Zubairi S, Huber R, Gordin F. Bacterial contamination of computer keyboards in a teaching hospital. Infect Control Hosp Epidemiol 2003; 24(4): Gray J, Mc Nicholl B, Webb H, Hogg G. Mice in the emergency department: vector for infection or technological aid? Eur J Emerg Med 2007;14(3): Kei J, Richards JR. The prevalence of methicillinresistant Staphylococcus aureus on inanimate objects in an Urban Emergency Department. J Emerg Med 2011;41(2): Grol R, Grimshaw J. From best evidence to best practice: effective implementation of change in patients' care. Lancet 2003;362(9391): Pittet D, Allegranzi B, Sax H, Dharan S, Pessoa-Silva CL, Donaldson L, et al. Evidence-based model for hand transmission during patient care and the role of improved practices. Lancet Infect Dis 2006;6(10): Boyce JM, Pittet D, Healthcare Infection Control Practices Advisory Committee, HICPAC/SHEA/APIC/ IDSA Hand Hygiene Task Force. Guideline for hand hygiene in health-care settings. MMWR Recomm Rep 2002;51(RR-16): Saint S, Bartoloni A, Virgili G, Mannelli F, Fumagalli S, di Martino P, et al. Marked variability in adherence to hand hygiene: a 5-unit observational study in Tuscany. Am J Infect Control 2009;37(4): Martin ET, Qin X, Baden H, Migita R, Zerr DM. Randomized double-blind crossover trial of ultraviolet light-sanitized keyboards in a pediatric hospital. Am J Infect Control 2011;39(5): Sweeney CP, Dancer SJ. Can hospital computers be disinfected using a hand-held UV light source? J Hosp Infect 2009;72(1): Neely AN, Maley MP. Dealing with contaminated computer keyboards and microbial survival. Am J Infect Control 2001;29(2): Braddy CM, Blair JE. Colonization of personal digital assistants used in a health care setting. Am J Infect Control 2005;33(4): Neely AN, Weber JM, Daviau P, MacGregor A, Miranda C, Nell M, et al. Computer equipment used in patient care within a multihospital system: recommendations for cleaning and disinfection. Am J Infect Control 2005;33(4): Rutala WA, White MS, Gergen MF, Weber DJ. Bacterial contamination of keyboards: efficacy and functional impact of disinfectants. Infect Control Hosp Epidemiol 2006;27(4):372-7.

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