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Contamination of healthcare workers' hands with bacterial spores
J Infect Chemother xxx (2016) 1e5
Contents lists available at ScienceDirect
Journal of Infection and Chemotherapy journal homepage: http://www.elsevier.com/locate/jic
Original article
Contamination of healthcare workers' hands with bacterial spores Teppei Sasahara a, b, *, Ryusuke Ae c, Michiyo Watanabe b, Yumiko Kimura d, Chikara Yonekawa e, Shunji Hayashi f, Yuji Morisawa b a
Department of Infection and Immunity, School of Medicine, Jichi Medical University, Tochigi, Japan Center for Infectious Diseases, Jichi Medical University Hospital, Tochigi, Japan c Division of Public Health, School of Medicine, Jichi Medical University, Tochigi, Japan d Division of Microbiology Laboratory, Jichi Medical University Hospital, Tochigi, Japan e Department of Emergency Medicine, School of Medicine, Jichi Medical University, Tochigi, Japan f Division of Microbiology, School of Medicine, Kitasato University, Kanagawa, Japan b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 23 March 2016 Received in revised form 21 April 2016 Accepted 25 April 2016 Available online xxx
Clostridium species and Bacillus spp. are spore-forming bacteria that cause hospital infections. The spores from these bacteria are transmitted from patient to patient via healthcare workers' hands. Although alcohol-based hand rubbing is an important hand hygiene practice, it is ineffective against bacterial spores. Therefore, healthcare workers should wash their hands with soap when they are contaminated with spores. However, the extent of health care worker hand contamination remains unclear. The aim of this study is to determine the level of bacterial spore contamination on healthcare workers' hands. The hands of 71 healthcare workers were evaluated for bacterial spore contamination. Spores attached to subject's hands were quantitatively examined after 9 working hours. The relationship between bacterial spore contamination and hand hygiene behaviors was also analyzed. Bacterial spores were detected on the hands of 54 subjects (76.1%). The mean number of spores detected was 468.3 CFU/hand (maximum: 3300 CFU/hand). Thirty-seven (52.1%) and 36 (50.7%) subjects were contaminated with Bacillus subtilis and Bacillus cereus, respectively. Nineteen subjects (26.8%) were contaminated with both Bacillus species. Clostridium difficile was detected on only one subject's hands. There was a significant negative correlation between the hand contamination level and the frequency of handwashing (r ¼ 0.44, P < 0.01) and a significant positive correlation between the hand contamination level and the elapsed time since last handwashing (r ¼ 0.34, P < 0.01). Healthcare workers' hands may be frequently contaminated with bacterial spores due to insufficient handwashing during daily patient care. © 2016 Japanese Society of Chemotherapy and The Japanese Association for Infectious Diseases. Published by Elsevier Ltd. All rights reserved.
Keywords: Clostridium Bacillus Bacterial spore Hand hygiene Handwashing Alcohol-based hand rubbing
1. Introduction Healthcare workers' hands can transmit pathogenic microorganisms between patients in medical facilities; therefore, healthcare workers are always required to keep their hands clean [1e3]. Alcohol-based hand rubbing is the most common routine hand hygiene practice, can be easily performed anywhere at any time, and removes pathogenic microorganisms from hands effectively and quickly [4,5]. However, alcohol-based hand rubbing is not enough to prevent hand contamination by every microorganism.
* Corresponding author. Department of Infection and Immunity, School of Medicine, Jichi Medical University, 3311-1 Yakushiji, Shimotsuke, Tochigi 329-0498, Japan. Tel.: þ81 285-58-7332; fax: þ81 285-44-1175. E-mail address: [email protected] (T. Sasahara).
For example, bacteria that form bacterial spores (i.e. Clostridium species and Bacillus spp.) are highly resistant to alcohol disinfectants [6]. Therefore, alcohol-based hand rubbing is ineffective against contamination with bacterial spores [7e10]. Spore-forming bacteria such as Clostridium difficile, Bacillus cereus, and Bacillus subtilis can cause hospital infections and nosocomial outbreaks [11e17]. Therefore, healthcare workers should wash their hands with soap when their hands are contaminated with these bacteria [7e10]. However, many healthcare workers think that hand contamination with spore-forming bacteria is less important than contamination with other pathogenic microorganisms, such as Staphylococcus aureus, Enterococcus spp., or gram-negative bacteria. Furthermore, the extent of healthcare worker hand contamination with bacterial spores remains unclear. Therefore, in this study, we evaluated the level of bacterial spore contamination on healthcare
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Please cite this article in press as: Sasahara T, et al., Contamination of healthcare workers' hands with bacterial spores, J Infect Chemother (2016), http://dx.doi.org/10.1016/j.jiac.2016.04.007
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T. Sasahara et al. / J Infect Chemother xxx (2016) 1e5
workers' hands. We also analyzed the relationship between bacterial spore contamination and hand hygiene behaviors. 2. Materials and methods This study was conducted from April 01 to August 31 2013 in the emergency medicine ward of Jichi Medical University Hospital, a tertiary hospital with 1132 beds. Various types of emergency patients, including trauma patients, have been admitted to this word. Seventy-one healthcare workers (61 nurses, 10 doctors) were invited to participate in this evaluation. Because this evaluation was conducted as a part of an infection control and hand hygiene education campaign in this ward, most of the nurses and the doctors on duty participated in this evaluation. Informed consent was obtained from all subjects. This study was approved by the institutional ethics committee of Jichi Medical University (No. 15-152). Bacterial spores attached to subject's hands were quantitatively evaluated after 9 working hours. The hand hygiene behavior (i.e. the frequency of alcohol-based hand rubbing, the elapsed time between last alcohol-based hand rubbing and sampling, the frequency of handwashing, and the elapsed time between last handwashing and sampling) of each subject during the past 9 working hours was assessed by study examiners. Staff on day duty was included in the evaluation. Subjects counted the frequency of alcohol-based hand rubbing or handwashing, and they recorded the last time of alcohol-based hand rubbing or handwashing on their own. Then they reported the findings of their hand hygiene behavior to the examiners. Two members of our infection control team acted as the examiners. GOJO™ (GOJO Industries, Inc., Akron, OH, USA) and Purerubbing™ (Air Liquide Co., Paris, France) were used for alcohol-based hand rubbing at our hospital. Bacterial spores were recovered from both of the subjects' hands by using the glove juice method [18,19]. The subjects' hands were inserted into sterile polyvinyl chloride gloves (JMS, Tokyo, Japan) containing 25 mL of sampling solution (0.04% KH2PO4, 1.01% Na2HPO4, and 0.10% Triton X-100), and the gloved hands were massaged for 1 min. Solutions were collected from the gloves and heated at 80 C for 20 min to eradicate vegetative form microorganisms other than bacterial spores. The solutions were then diluted 10-fold with sterile saline, and the diluents were inoculated onto agar medium plates. Mannitol Egg Yolk Polymyxin (MYP) agar plates (Becton Dickinson and Co., Franklin Lakes, NJ, USA) were used for Bacillus spp., and cycloserine-cefoxitin-fructose agar (CCFA) plates (Becton Dickinson and Co.) were used for C. difficile. After inoculation, the MYP agar plates were incubated at 37 C under aerobic conditions for 12 h, and the CCFA plates were incubated at 37 C under anaerobic conditions for 48 h. The numbers of colonies on the plates were then counted. Mannitol-positive, lecithinase-negative, large, yellow, wrinkle-surfaced colonies on MYP agar plates were identified as B. subtilis, and Mannitol-negative, lecithinase-positive, large, flat, granular colonies on MYP agar plates were identified as B. cereus [20,21]. Colonies that were yellow, circular with a slightly filamentous edge, lipase-negative, lecithinase-negative, and had a flat to low umbonate in profile and a ground-glass appearance on CCFA plates were identified as C. difficile [22]. The contamination of subjects' hands with transient bacteria other than spore-forming bacteria was also evaluated. Gramnegative bacteria and Enterococcus spp. were recovered from the hands using the glove juice method as described above. The solutions containing bacteria were diluted 10-fold with sterile saline without heating, and the diluents were inoculated onto agar medium plates. MacConkey agar plates (Becton Dickinson and Co.) were used for gram-negative bacteria, and Enterococcosel agar plates (Becton Dickinson and Co.) were used for Enterococcus spp.
After inoculation, these agar plates were incubated at 37 C under aerobic conditions for 12 h, and the numbers of colonies on the plates were counted. Species identification of the colonies was determined using an automated system for microbial identification (Vitek 2 system; SYSMEX bioMerieux Co. Ltd., Tokyo, Japan). All analyses were performed using SPSS Statistics software (IBM SPSS Statistics version 19 for Windows; IBM Corp, NY, USA). A Student's t-test was used to compare two groups (nurses and doctors) of data. The significance threshold was set at 0.05. We assessed the correlations between the degree of hand contamination and hand hygiene behavior using a Pearson productemoment correlation coefficient. The minimum detection threshold for bacterial sampling in this study was 25 CFU/hand. 3. Results The level of bacterial spore contamination found on the hands of the 71 subjects is shown in Fig. 1. Bacterial spores were detected on the hands of 54 subjects (76.1%) and the mean number of bacterial spores was 468.3 CFU/hand (maximum: 3300 CFU/hand). In addition, the hands of all doctors were contaminated with bacterial spores. The hands of 37 subjects (52.1%) were contaminated with B. subtilis (mean: 307.0 CFU/hand, maximum: 3000 CFU/hand), the hands of 36 subjects (50.7%) were contaminated with B. cereus (mean: 138.5 CFU/hand, maximum: 1000 CFU/hand), and the hands of 19 subjects (26.8%) were contaminated with both species of Bacillus. Meanwhile, C. difficile was detected on only one subject's hands (1.4%) and the contamination level was low (50 CFU/hand). There was no significant difference between the bacterial spore contamination level on the hands of the nurses and the hands of the doctors (P ¼ 0.27). Gram-negative bacteria and Enterococcus spp. were detected on only 14 subjects' hands (19.7%). Pseudomonas spp. were detected on nine (13.7%, mean: 155.6 CFU/hand), Escherichia coli on three (4.2%, Mean 41.7 CFU/hand), Klebsiella oxytoca on one (1.4%, 325 CFU/ hand), and Enterococcus faecalis on one (1.4%, 300 CFU/hand).
Fig. 1. Bacterial spore hand contamination among healthcare workers. Data are displayed as a box-and-whisker plot and include the smallest value observed, lower quartile, median, upper quartile, and largest value observed. Black points indicate outliers or single points.
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T. Sasahara et al. / J Infect Chemother xxx (2016) 1e5
Table 1 shows the hand hygiene behaviors of the subjects. The mean frequency of alcohol-based hand rubbing was 4.1 ± 3.3 times/ hour among the total sample. The mean frequency of alcohol-based hand rubbing among the nurses was 4.4 ± 3.4 times/hour, which was significantly higher (P < 0.01) than that of the doctors (2.2 ± 0.9 times/hour). The mean elapsed time between the last alcoholbased hand rubbing and sampling among the total sample was 25.6 ± 41.0 min. The mean elapsed time between the last alcoholbased hand rubbing and sampling among the doctors was 83.4 ± 80.0 min, which was significantly longer (P ¼ 0.01) than that of the nurses (16.2 ± 18.9 min). The mean frequency of handwashing was 10.6 ± 6.8 times/9 h among the total sample. There was no significant difference between the frequency of handwashing among the nurses (10.9 ± 7.3 times/9 h) and among the doctors (8.8 ± 3.0 times/9 h) (P ¼ 0.06). The mean elapsed time between the last handwashing and sampling among the total sample was 33.8 ± 60.6 min. There was no significant difference between the elapsed time since last handwashing among the nurses (33.9 ± 61.9 times/9 h) and among the doctors (33.2 ± 55.0 times/9 h) (P ¼ 0.49). Table 2 shows the correlation between hand hygiene behavior and the hand contamination level with bacterial spores. There was no significant correlation between the hand contamination level and the frequency of alcohol-based hand rubbing (r ¼ 0.10, P ¼ 0.41) or between the hand contamination level and the elapsed time since last alcohol-based hand rubbing (r ¼ 0.01, P ¼ 0.95). However, there was significant negative correlation between the hand contamination level and the frequency of handwashing (r ¼ 0.44, P < 0.01) and a significant positive correlation between the hand contamination level and the elapsed time since last handwashing (r ¼ 0.34, P < 0.01) (Fig. 2). 4. Discussion Hand contamination is one of the most common sources of healthcare associated infections, and healthcare workers hands are frequently contaminated with pathogenic bacteria (such as Staphylococcus spp., Pseudomonas spp., Enterococcus spp., Acinetobacter spp., and Enterobacteriaceae) during routine patient care [23e26]. Therefore, current infection control guidelines emphasize the importance of hand hygiene as the most effective measure to reduce hand contamination [1e5]. However, alcohol-based hand rubbing is not effective against contamination with bacterial spores [6]. Although many healthcare workers do not recognize the importance of spore-forming bacteria, recent studies have reported that microorganisms such as C. difficile and Bacillus spp. cause healthcare associated infections among inpatients and suggest that
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healthcare workers should prevent hand contamination by the spore-forming bacteria [11e17]. However, the level of hand contamination remains unclear. Therefore, our study aimed to quantitatively evaluate hand contamination with bacterial spores. In our study, bacterial spores were detected on the hands of 76.1% of healthcare workers who participated in this evaluation. Although the contamination level was low among the majority of subjects (Fig. 1), the hands of some subjects were highly contaminated with the spores (maximum: 3300 CFU/hand), and the majority of the bacterial spores belonged to the Bacillus spp. For example, B. subtilis and B. cereus were distributed among half of the subjects, and approximately one-quarter of the subjects were contaminated with both Bacillus species. These results suggest that healthcare workers' hands usually become contaminated with bacterial spores, mainly Bacillus spores, during clinical practice. This may pose a threat to infection control because healthcare workers hands contaminated with Bacillus spores can cause a nosocomial outbreak [15,16]. In addition, although the contamination level was low in most cases, some healthcare workers may transmit a large number of bacterial spores to patients via their hands; therefore, it is better if healthcare workers prevent hand contamination with spores as much as possible. Conversely, even though multiple nurses and doctors cared for a patient with a C. difficile infection, a small amount of C. difficile spores (50 CFU/hand) was detected from only one subject who had cared for this patient. However, healthcare workers' hands are generally considered the primary means of transmission of C. difficile spores in medical facilities, and the contamination of healthcare workers' hands with C. difficile spores during the care of patients with C. difficile infections has been reported [27,28]. In particular, Landelle et al. showed that nearly one-quarter of healthcare workers have hands contaminated with C. difficile spores after routine care of patients with C. difficile infections [27]. The low proportion of the healthcare workers in our study who had C. difficile contaminated hands may be explained by adherence to precautions against C. difficile infections, including wearing gloves during patient care. Furthermore, gram-negative bacteria and Enterococcus spp. were detected from only 14 subjects' hands (19.7%), and the contamination levels were also low. Thus, in our study, contamination with common transient bacteria was found less often than contamination with spore-forming bacteria. Therefore, although adequate alcohol-based hand rubbing might reduce contamination with common transient bacteria, it might not prevent contamination with bacterial spores [29]. In addition, other studies have suggested that compliance with hand hygiene procedures is relatively low among doctors when compared to nurses [30,31]. Similarly, in our study, the frequency of
Table 1 Hand hygiene behaviors among the subjects. Total sample
Hand hygiene behavior Alcohol-based hand-rubbing
Nurses
Mean frequency
Mean elapsed time from last hand hygiene procedure (minutes)
4.1 ± 3.3 (times/hour)
25.6 ± 41.0
Mean frequency
Doctors Mean elapsed time from last hand hygiene procedure (minutes)
4.4 ± 3.4 (times/hour)
Mean frequency
10.6 ± 6.8 (times/9 h)
Mean elapsed time from last hand hygiene procedure (minutes)
2.2 ± 0.9 (times/hour) 16.2 ± 18.9
Handwashing
P Value
<0.01 83.4 ± 80.0
0.01
33.8 ± 60.6 10.9 ± 7.3 (times/9 h)
8.8 ± 3.0 (times/9 h) 33.9 ± 61.9
0.06 33.2 ± 55.0
0.49
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Table 2 Correlation between hand hygiene behavior and the hand contamination level with bacterial spores. Pearson's correlation coefficient (r) Frequency of alcohol-based hand-rubbing Elapsed time since last a lcohol-based hand-rubbing Frequency of handwashing Elapsed time since last handwashing
P Value
0.10
0.41
0.01
0.95
0.44
<0.01
0.34
<0.01
alcohol-based hand rubbing among the doctors was lower than that of the nurses. However, we found no significant difference between the frequency of handwashing among the nurses and among the doctors. Thus, nurses might perform alcohol-based hand rubbing more diligently than doctors, but nurses as well as doctors might place less importance on handwashing than other hand hygiene practices. Our results also revealed that there was no significant correlation between hand contamination with bacterial spores and the frequency of alcohol-based hand rubbing or between hand contamination with bacterial spores and the elapsed time since last alcohol-based hand rubbing. Thus, hand hygiene behaviors such as alcohol-based hand rubbing might not affect hand contamination with bacterial spores. However, there was a significant negative correlation between the hand contamination level and the frequency of handwashing and a significant positive correlation between the hand contamination level and the elapsed time since last handwashing. These results suggest that more frequent handwashing prevents spore contamination of the hands and indicate that contamination levels increase over time. Therefore, healthcare workers should wash their hands frequently in addition to performing alcohol-based hand rubbing. In our study, the spore contamination level of hands that were washed more than 11 times over 9 h was low (Fig. 2). Thus, if possible, healthcare workers should wash their hands more than twice per hour in order to prevent hand contamination with bacterial spores.
Fig. 2. The relationship between the bacterial spore hand contamination levels and the frequency of handwashing. A correlation diagram representing the relationship between the hand contamination levels with bacterial spores and the frequency of handwashing. A significant negative correlation was found (correlation coefficient: r ¼ 0.44).
A major limitation of this study is that hand hygiene behaviors were not confirmed by direct observation, and the evaluation of hand hygiene behavior as recalled by the subjects might undermine the credibility of the results. However, hand contamination with bacterial spores was accurately measured, and the results regarding the relationship between bacterial spore contamination and hand hygiene behavior can teach us a great deal about daily infection control strategies. Additionally, our study was only conducted in the emergency medicine ward. The outcome may be affected by characteristics of the ward and the severity of patients' conditions. Further studies targeted at healthcare workers at various types of wards are needed. The results of our study suggest that healthcare workers' hands are commonly contaminated with bacterial spores during daily patient care, and that contamination persists under insufficient handwashing. Therefore, healthcare workers should emphasize handwashing as well as alcohol-based hand rubbing as routine hand hygiene practice. Conflict of interest None. Funding sources This work was supported by JSPS KAKENHI Grant Number 25860482. References [1] 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. Recommendations of the healthcare infection control practices advisory committee and the HICPAC/SHEA/APIC/IDSA hand hygiene task force. MMWR Recomm Rep 2002;51:1e45. [2] Pratt RJ, Pellowe CM, Wilson JA, Loveday HP, Harper PJ, Jones SR, et al. epic2: national evidence-based guidelines for preventing healthcare-associated infections in NHS hospitals in England. J Hosp Infect 2007;65:S1e64. [3] 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;30:611e22. [4] Guilhermetti M, Marques Wiirzler LA, Castanheira Facio B, da Silva Furlan M, Campo Meschial W, Bronharo Tognim MC, et al. Antimicrobial efficacy of alcohol-based hand gels. J Hosp Infect 2010;74:219e24. [5] Girou E, Loyeau S, Legrand P, Oppein F, Brun-Buisson C. Efficacy of handrubbing with alcohol based solution versus standard handwashing with antiseptic soap: randomised clinical trial. BMJ 2002;325:362e6. [6] Russell AD. Bacterial spores and chemical sporicidal agents. Clin Microbiol Rev 1990;3:99e119. [7] Oughton MT, Loo VG, Dendukuri N, Fenn S, Libman MD. Hand hygiene with soap and water is superior to alcohol rub and antiseptic wipes for removal of Clostridium difficile. Infect Control Hosp Epidemiol 2009;30:939e44. [8] Jabbar U, Leischner J, Kasper D, Gerber R, Sambol SP, Parada JP, et al. Effectiveness of alcohol-based hand rubs for removal of Clostridium difficile spores from hands. Infect Control Hosp Epidemiol 2010;31:565e70. [9] Weber DJ, Sickbert-Bennett E, Gergen MF, Rutala WA. Efficacy of selected hand hygiene agents used to remove Bacillus atrophaeus (a surrogate of Bacillus anthracis) from contaminated hands. JAMA 2003;289:1274e7. [10] Sasahara T, Hayashi S, Hosoda K, Morisawa Y, Hirai Y. Comparison of hand hygiene procedures for removing Bacillus cereus spores. Biocontrol Sci 2014;19:129e34. [11] Freeman J, Bauer MP, Baines SD, Corver J, Fawley WN, Goorhuis B, et al. The changing epidemiology of Clostridium difficile infections. Clin Microbiol Rev 2010;23:529e49. [12] McFarland LV, Mulligan ME, Kwok RY, Stamm WE. Nosocomial acquisition of Clostridium difficile infection. N Engl J Med 1989;320:204e10. [13] Richard V, Van der Auwera P, Snoeck R, Daneau D, Meunier F. Nosocomial bacteremia caused by Bacillus species. Eur J Clin Microbiol Infect Dis 1988;7: 783e5. [14] Matsumoto S, Suenaga H, Naito K, Sawazaki M, Hiramatsu T, Agata N. Management of suspected nosocomial infection: an audit of 19 hospitalized patients with septicemia caused by Bacillus species. Jpn J Infect Dis 2000;53: 196e202.
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T. Sasahara et al. / J Infect Chemother xxx (2016) 1e5 [15] Van Der Zwet WC, Parlevliet GA, Savelkoul PH, Stoof J, Kaiser AM, Van Furth AM, et al. Outbreak of Bacillus cereus infections in a neonatal intensive care unit traced to balloons used in manual ventilation. J Clin Microbiol 2000;38:4131e6. [16] Sasahara T, Hayashi S, Morisawa Y, Sakihama T, Yoshimura A, Hirai Y. Bacillus cereus bacteremia outbreak due to contaminated hospital linens. Eur J Clin Microbiol Infect Dis 2011;30:219e26. [17] Balm MN, Jureen R, Teo C, Yeoh AE, Lin RT, Dancer SJ, et al. Hot and steamy: outbreak of Bacillus cereus in Singapore associated with construction work and laundry practices. J Hosp Infect 2012;81:224e30. [18] United States Food and Drug Administration. Effectiveness testing of surgical hand scrub (glove juice test). Fed Regist 1974;39:33137e8. [19] United States Food and Drug Administration. Effectiveness testing of surgical hand scrub (glove juice test). Fed Regist 1978;43:1242e3. [20] Tallent SM, Kotewicz KM, Strain EA, Bennett RW. Efficient isolation and identification of Bacillus cereus group. J AOAC Int 2012;95:446e51. [21] Mossel DA, Koopman MJ, Jongerius E. Enumeration of Bacillus cereus in foods. Appl Microbiol 1967;15:650e3. [22] George WL, Sutter VL, Citron D, Finegold SM. Selective and differential medium for isolation of Clostridium difficile. J Clin Microbiol 1979;9:214e9. pez ML, Riera M, Font R, Nicol [23] Monistrol O, Lo as C, Escobar MA, et al. Hand contamination during routine care in medical wards: the role of hand hygiene compliance. J Med Microbiol 2013;62:623e9. [24] Naeem A, Saluja SA, Krishna D, Shitanshu M, Arun S, Taseer B. Contamination of dentist's Hands with and without finger rings. J Int Oral Health 2015;7: 114e7.
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[25] Salmon S, Truong AT, Nguyen VH, Pittet D, McLaws ML. Health care workers' hand contamination levels and antibacterial efficacy of different hand hygiene methods used in a Vietnamese hospital. Am J Infect Control 2014;42:178e81. [26] Munoz-Price LS, Arheart KL, Mills JP, Cleary T, Depascale D, Jimenez A, et al. Associations between bacterial contamination of health care workers' hands and contamination of white coats and scrubs. Am J Infect Control 2012;40: e245e8. [27] Guerrero DM, Nerandzic MM, Jury LA, Jinno S, Chang S, Donskey CJ. Acquisition of spores on gloved hands after contact with the skin of patients with Clostridium difficile infection and with environmental surfaces in their rooms. Am J Infect Control 2012;40:556e8. [28] Landelle C, Verachten M, Legrand P, Girou E, Barbut F, Brun-Buisson C. Contamination of healthcare workers' hands with Clostridium difficile spores after caring for patients with C. difficile infection. Infect Control Hosp Epidemiol 2014;35:10e5. [29] Ojaj€ arvi J. Effectiveness of hand washing and disinfection methods in removing transient bacteria after patient nursing. J Hyg (Lond) 1980;85: 193e203. [30] Pittet D, Hugonnet S, Harbarth S, Mourouga P, Sauvan V, Touveneau S, et al. Effectiveness of a hospital-wide programme to improve compliance with hand hygiene. Infection Control Programme. Lancet 2000;356:1307e12. [31] Duggan JM, Hensley S, Khuder S, Papadimos TJ, Jacobs L. Inverse correlation between level of professional education and rate of handwashing compliance in a teaching hospital. Infect Control Hosp Epidemiol 2008;29:534e8.
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Contents lists available at ScienceDirect
Journal of Infection and Chemotherapy journal homepage: http://www.elsevier.com/locate/jic
Original article
Contamination of healthcare workers' hands with bacterial spores Teppei Sasahara a, b, *, Ryusuke Ae c, Michiyo Watanabe b, Yumiko Kimura d, Chikara Yonekawa e, Shunji Hayashi f, Yuji Morisawa b a
Department of Infection and Immunity, School of Medicine, Jichi Medical University, Tochigi, Japan Center for Infectious Diseases, Jichi Medical University Hospital, Tochigi, Japan c Division of Public Health, School of Medicine, Jichi Medical University, Tochigi, Japan d Division of Microbiology Laboratory, Jichi Medical University Hospital, Tochigi, Japan e Department of Emergency Medicine, School of Medicine, Jichi Medical University, Tochigi, Japan f Division of Microbiology, School of Medicine, Kitasato University, Kanagawa, Japan b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 23 March 2016 Received in revised form 21 April 2016 Accepted 25 April 2016 Available online xxx
Clostridium species and Bacillus spp. are spore-forming bacteria that cause hospital infections. The spores from these bacteria are transmitted from patient to patient via healthcare workers' hands. Although alcohol-based hand rubbing is an important hand hygiene practice, it is ineffective against bacterial spores. Therefore, healthcare workers should wash their hands with soap when they are contaminated with spores. However, the extent of health care worker hand contamination remains unclear. The aim of this study is to determine the level of bacterial spore contamination on healthcare workers' hands. The hands of 71 healthcare workers were evaluated for bacterial spore contamination. Spores attached to subject's hands were quantitatively examined after 9 working hours. The relationship between bacterial spore contamination and hand hygiene behaviors was also analyzed. Bacterial spores were detected on the hands of 54 subjects (76.1%). The mean number of spores detected was 468.3 CFU/hand (maximum: 3300 CFU/hand). Thirty-seven (52.1%) and 36 (50.7%) subjects were contaminated with Bacillus subtilis and Bacillus cereus, respectively. Nineteen subjects (26.8%) were contaminated with both Bacillus species. Clostridium difficile was detected on only one subject's hands. There was a significant negative correlation between the hand contamination level and the frequency of handwashing (r ¼ 0.44, P < 0.01) and a significant positive correlation between the hand contamination level and the elapsed time since last handwashing (r ¼ 0.34, P < 0.01). Healthcare workers' hands may be frequently contaminated with bacterial spores due to insufficient handwashing during daily patient care. © 2016 Japanese Society of Chemotherapy and The Japanese Association for Infectious Diseases. Published by Elsevier Ltd. All rights reserved.
Keywords: Clostridium Bacillus Bacterial spore Hand hygiene Handwashing Alcohol-based hand rubbing
1. Introduction Healthcare workers' hands can transmit pathogenic microorganisms between patients in medical facilities; therefore, healthcare workers are always required to keep their hands clean [1e3]. Alcohol-based hand rubbing is the most common routine hand hygiene practice, can be easily performed anywhere at any time, and removes pathogenic microorganisms from hands effectively and quickly [4,5]. However, alcohol-based hand rubbing is not enough to prevent hand contamination by every microorganism.
* Corresponding author. Department of Infection and Immunity, School of Medicine, Jichi Medical University, 3311-1 Yakushiji, Shimotsuke, Tochigi 329-0498, Japan. Tel.: þ81 285-58-7332; fax: þ81 285-44-1175. E-mail address: [email protected] (T. Sasahara).
For example, bacteria that form bacterial spores (i.e. Clostridium species and Bacillus spp.) are highly resistant to alcohol disinfectants [6]. Therefore, alcohol-based hand rubbing is ineffective against contamination with bacterial spores [7e10]. Spore-forming bacteria such as Clostridium difficile, Bacillus cereus, and Bacillus subtilis can cause hospital infections and nosocomial outbreaks [11e17]. Therefore, healthcare workers should wash their hands with soap when their hands are contaminated with these bacteria [7e10]. However, many healthcare workers think that hand contamination with spore-forming bacteria is less important than contamination with other pathogenic microorganisms, such as Staphylococcus aureus, Enterococcus spp., or gram-negative bacteria. Furthermore, the extent of healthcare worker hand contamination with bacterial spores remains unclear. Therefore, in this study, we evaluated the level of bacterial spore contamination on healthcare
http://dx.doi.org/10.1016/j.jiac.2016.04.007 1341-321X/© 2016 Japanese Society of Chemotherapy and The Japanese Association for Infectious Diseases. Published by Elsevier Ltd. All rights reserved.
Please cite this article in press as: Sasahara T, et al., Contamination of healthcare workers' hands with bacterial spores, J Infect Chemother (2016), http://dx.doi.org/10.1016/j.jiac.2016.04.007
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T. Sasahara et al. / J Infect Chemother xxx (2016) 1e5
workers' hands. We also analyzed the relationship between bacterial spore contamination and hand hygiene behaviors. 2. Materials and methods This study was conducted from April 01 to August 31 2013 in the emergency medicine ward of Jichi Medical University Hospital, a tertiary hospital with 1132 beds. Various types of emergency patients, including trauma patients, have been admitted to this word. Seventy-one healthcare workers (61 nurses, 10 doctors) were invited to participate in this evaluation. Because this evaluation was conducted as a part of an infection control and hand hygiene education campaign in this ward, most of the nurses and the doctors on duty participated in this evaluation. Informed consent was obtained from all subjects. This study was approved by the institutional ethics committee of Jichi Medical University (No. 15-152). Bacterial spores attached to subject's hands were quantitatively evaluated after 9 working hours. The hand hygiene behavior (i.e. the frequency of alcohol-based hand rubbing, the elapsed time between last alcohol-based hand rubbing and sampling, the frequency of handwashing, and the elapsed time between last handwashing and sampling) of each subject during the past 9 working hours was assessed by study examiners. Staff on day duty was included in the evaluation. Subjects counted the frequency of alcohol-based hand rubbing or handwashing, and they recorded the last time of alcohol-based hand rubbing or handwashing on their own. Then they reported the findings of their hand hygiene behavior to the examiners. Two members of our infection control team acted as the examiners. GOJO™ (GOJO Industries, Inc., Akron, OH, USA) and Purerubbing™ (Air Liquide Co., Paris, France) were used for alcohol-based hand rubbing at our hospital. Bacterial spores were recovered from both of the subjects' hands by using the glove juice method [18,19]. The subjects' hands were inserted into sterile polyvinyl chloride gloves (JMS, Tokyo, Japan) containing 25 mL of sampling solution (0.04% KH2PO4, 1.01% Na2HPO4, and 0.10% Triton X-100), and the gloved hands were massaged for 1 min. Solutions were collected from the gloves and heated at 80 C for 20 min to eradicate vegetative form microorganisms other than bacterial spores. The solutions were then diluted 10-fold with sterile saline, and the diluents were inoculated onto agar medium plates. Mannitol Egg Yolk Polymyxin (MYP) agar plates (Becton Dickinson and Co., Franklin Lakes, NJ, USA) were used for Bacillus spp., and cycloserine-cefoxitin-fructose agar (CCFA) plates (Becton Dickinson and Co.) were used for C. difficile. After inoculation, the MYP agar plates were incubated at 37 C under aerobic conditions for 12 h, and the CCFA plates were incubated at 37 C under anaerobic conditions for 48 h. The numbers of colonies on the plates were then counted. Mannitol-positive, lecithinase-negative, large, yellow, wrinkle-surfaced colonies on MYP agar plates were identified as B. subtilis, and Mannitol-negative, lecithinase-positive, large, flat, granular colonies on MYP agar plates were identified as B. cereus [20,21]. Colonies that were yellow, circular with a slightly filamentous edge, lipase-negative, lecithinase-negative, and had a flat to low umbonate in profile and a ground-glass appearance on CCFA plates were identified as C. difficile [22]. The contamination of subjects' hands with transient bacteria other than spore-forming bacteria was also evaluated. Gramnegative bacteria and Enterococcus spp. were recovered from the hands using the glove juice method as described above. The solutions containing bacteria were diluted 10-fold with sterile saline without heating, and the diluents were inoculated onto agar medium plates. MacConkey agar plates (Becton Dickinson and Co.) were used for gram-negative bacteria, and Enterococcosel agar plates (Becton Dickinson and Co.) were used for Enterococcus spp.
After inoculation, these agar plates were incubated at 37 C under aerobic conditions for 12 h, and the numbers of colonies on the plates were counted. Species identification of the colonies was determined using an automated system for microbial identification (Vitek 2 system; SYSMEX bioMerieux Co. Ltd., Tokyo, Japan). All analyses were performed using SPSS Statistics software (IBM SPSS Statistics version 19 for Windows; IBM Corp, NY, USA). A Student's t-test was used to compare two groups (nurses and doctors) of data. The significance threshold was set at 0.05. We assessed the correlations between the degree of hand contamination and hand hygiene behavior using a Pearson productemoment correlation coefficient. The minimum detection threshold for bacterial sampling in this study was 25 CFU/hand. 3. Results The level of bacterial spore contamination found on the hands of the 71 subjects is shown in Fig. 1. Bacterial spores were detected on the hands of 54 subjects (76.1%) and the mean number of bacterial spores was 468.3 CFU/hand (maximum: 3300 CFU/hand). In addition, the hands of all doctors were contaminated with bacterial spores. The hands of 37 subjects (52.1%) were contaminated with B. subtilis (mean: 307.0 CFU/hand, maximum: 3000 CFU/hand), the hands of 36 subjects (50.7%) were contaminated with B. cereus (mean: 138.5 CFU/hand, maximum: 1000 CFU/hand), and the hands of 19 subjects (26.8%) were contaminated with both species of Bacillus. Meanwhile, C. difficile was detected on only one subject's hands (1.4%) and the contamination level was low (50 CFU/hand). There was no significant difference between the bacterial spore contamination level on the hands of the nurses and the hands of the doctors (P ¼ 0.27). Gram-negative bacteria and Enterococcus spp. were detected on only 14 subjects' hands (19.7%). Pseudomonas spp. were detected on nine (13.7%, mean: 155.6 CFU/hand), Escherichia coli on three (4.2%, Mean 41.7 CFU/hand), Klebsiella oxytoca on one (1.4%, 325 CFU/ hand), and Enterococcus faecalis on one (1.4%, 300 CFU/hand).
Fig. 1. Bacterial spore hand contamination among healthcare workers. Data are displayed as a box-and-whisker plot and include the smallest value observed, lower quartile, median, upper quartile, and largest value observed. Black points indicate outliers or single points.
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Table 1 shows the hand hygiene behaviors of the subjects. The mean frequency of alcohol-based hand rubbing was 4.1 ± 3.3 times/ hour among the total sample. The mean frequency of alcohol-based hand rubbing among the nurses was 4.4 ± 3.4 times/hour, which was significantly higher (P < 0.01) than that of the doctors (2.2 ± 0.9 times/hour). The mean elapsed time between the last alcoholbased hand rubbing and sampling among the total sample was 25.6 ± 41.0 min. The mean elapsed time between the last alcoholbased hand rubbing and sampling among the doctors was 83.4 ± 80.0 min, which was significantly longer (P ¼ 0.01) than that of the nurses (16.2 ± 18.9 min). The mean frequency of handwashing was 10.6 ± 6.8 times/9 h among the total sample. There was no significant difference between the frequency of handwashing among the nurses (10.9 ± 7.3 times/9 h) and among the doctors (8.8 ± 3.0 times/9 h) (P ¼ 0.06). The mean elapsed time between the last handwashing and sampling among the total sample was 33.8 ± 60.6 min. There was no significant difference between the elapsed time since last handwashing among the nurses (33.9 ± 61.9 times/9 h) and among the doctors (33.2 ± 55.0 times/9 h) (P ¼ 0.49). Table 2 shows the correlation between hand hygiene behavior and the hand contamination level with bacterial spores. There was no significant correlation between the hand contamination level and the frequency of alcohol-based hand rubbing (r ¼ 0.10, P ¼ 0.41) or between the hand contamination level and the elapsed time since last alcohol-based hand rubbing (r ¼ 0.01, P ¼ 0.95). However, there was significant negative correlation between the hand contamination level and the frequency of handwashing (r ¼ 0.44, P < 0.01) and a significant positive correlation between the hand contamination level and the elapsed time since last handwashing (r ¼ 0.34, P < 0.01) (Fig. 2). 4. Discussion Hand contamination is one of the most common sources of healthcare associated infections, and healthcare workers hands are frequently contaminated with pathogenic bacteria (such as Staphylococcus spp., Pseudomonas spp., Enterococcus spp., Acinetobacter spp., and Enterobacteriaceae) during routine patient care [23e26]. Therefore, current infection control guidelines emphasize the importance of hand hygiene as the most effective measure to reduce hand contamination [1e5]. However, alcohol-based hand rubbing is not effective against contamination with bacterial spores [6]. Although many healthcare workers do not recognize the importance of spore-forming bacteria, recent studies have reported that microorganisms such as C. difficile and Bacillus spp. cause healthcare associated infections among inpatients and suggest that
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healthcare workers should prevent hand contamination by the spore-forming bacteria [11e17]. However, the level of hand contamination remains unclear. Therefore, our study aimed to quantitatively evaluate hand contamination with bacterial spores. In our study, bacterial spores were detected on the hands of 76.1% of healthcare workers who participated in this evaluation. Although the contamination level was low among the majority of subjects (Fig. 1), the hands of some subjects were highly contaminated with the spores (maximum: 3300 CFU/hand), and the majority of the bacterial spores belonged to the Bacillus spp. For example, B. subtilis and B. cereus were distributed among half of the subjects, and approximately one-quarter of the subjects were contaminated with both Bacillus species. These results suggest that healthcare workers' hands usually become contaminated with bacterial spores, mainly Bacillus spores, during clinical practice. This may pose a threat to infection control because healthcare workers hands contaminated with Bacillus spores can cause a nosocomial outbreak [15,16]. In addition, although the contamination level was low in most cases, some healthcare workers may transmit a large number of bacterial spores to patients via their hands; therefore, it is better if healthcare workers prevent hand contamination with spores as much as possible. Conversely, even though multiple nurses and doctors cared for a patient with a C. difficile infection, a small amount of C. difficile spores (50 CFU/hand) was detected from only one subject who had cared for this patient. However, healthcare workers' hands are generally considered the primary means of transmission of C. difficile spores in medical facilities, and the contamination of healthcare workers' hands with C. difficile spores during the care of patients with C. difficile infections has been reported [27,28]. In particular, Landelle et al. showed that nearly one-quarter of healthcare workers have hands contaminated with C. difficile spores after routine care of patients with C. difficile infections [27]. The low proportion of the healthcare workers in our study who had C. difficile contaminated hands may be explained by adherence to precautions against C. difficile infections, including wearing gloves during patient care. Furthermore, gram-negative bacteria and Enterococcus spp. were detected from only 14 subjects' hands (19.7%), and the contamination levels were also low. Thus, in our study, contamination with common transient bacteria was found less often than contamination with spore-forming bacteria. Therefore, although adequate alcohol-based hand rubbing might reduce contamination with common transient bacteria, it might not prevent contamination with bacterial spores [29]. In addition, other studies have suggested that compliance with hand hygiene procedures is relatively low among doctors when compared to nurses [30,31]. Similarly, in our study, the frequency of
Table 1 Hand hygiene behaviors among the subjects. Total sample
Hand hygiene behavior Alcohol-based hand-rubbing
Nurses
Mean frequency
Mean elapsed time from last hand hygiene procedure (minutes)
4.1 ± 3.3 (times/hour)
25.6 ± 41.0
Mean frequency
Doctors Mean elapsed time from last hand hygiene procedure (minutes)
4.4 ± 3.4 (times/hour)
Mean frequency
10.6 ± 6.8 (times/9 h)
Mean elapsed time from last hand hygiene procedure (minutes)
2.2 ± 0.9 (times/hour) 16.2 ± 18.9
Handwashing
P Value
<0.01 83.4 ± 80.0
0.01
33.8 ± 60.6 10.9 ± 7.3 (times/9 h)
8.8 ± 3.0 (times/9 h) 33.9 ± 61.9
0.06 33.2 ± 55.0
0.49
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T. Sasahara et al. / J Infect Chemother xxx (2016) 1e5
Table 2 Correlation between hand hygiene behavior and the hand contamination level with bacterial spores. Pearson's correlation coefficient (r) Frequency of alcohol-based hand-rubbing Elapsed time since last a lcohol-based hand-rubbing Frequency of handwashing Elapsed time since last handwashing
P Value
0.10
0.41
0.01
0.95
0.44
<0.01
0.34
<0.01
alcohol-based hand rubbing among the doctors was lower than that of the nurses. However, we found no significant difference between the frequency of handwashing among the nurses and among the doctors. Thus, nurses might perform alcohol-based hand rubbing more diligently than doctors, but nurses as well as doctors might place less importance on handwashing than other hand hygiene practices. Our results also revealed that there was no significant correlation between hand contamination with bacterial spores and the frequency of alcohol-based hand rubbing or between hand contamination with bacterial spores and the elapsed time since last alcohol-based hand rubbing. Thus, hand hygiene behaviors such as alcohol-based hand rubbing might not affect hand contamination with bacterial spores. However, there was a significant negative correlation between the hand contamination level and the frequency of handwashing and a significant positive correlation between the hand contamination level and the elapsed time since last handwashing. These results suggest that more frequent handwashing prevents spore contamination of the hands and indicate that contamination levels increase over time. Therefore, healthcare workers should wash their hands frequently in addition to performing alcohol-based hand rubbing. In our study, the spore contamination level of hands that were washed more than 11 times over 9 h was low (Fig. 2). Thus, if possible, healthcare workers should wash their hands more than twice per hour in order to prevent hand contamination with bacterial spores.
Fig. 2. The relationship between the bacterial spore hand contamination levels and the frequency of handwashing. A correlation diagram representing the relationship between the hand contamination levels with bacterial spores and the frequency of handwashing. A significant negative correlation was found (correlation coefficient: r ¼ 0.44).
A major limitation of this study is that hand hygiene behaviors were not confirmed by direct observation, and the evaluation of hand hygiene behavior as recalled by the subjects might undermine the credibility of the results. However, hand contamination with bacterial spores was accurately measured, and the results regarding the relationship between bacterial spore contamination and hand hygiene behavior can teach us a great deal about daily infection control strategies. Additionally, our study was only conducted in the emergency medicine ward. The outcome may be affected by characteristics of the ward and the severity of patients' conditions. Further studies targeted at healthcare workers at various types of wards are needed. The results of our study suggest that healthcare workers' hands are commonly contaminated with bacterial spores during daily patient care, and that contamination persists under insufficient handwashing. Therefore, healthcare workers should emphasize handwashing as well as alcohol-based hand rubbing as routine hand hygiene practice. Conflict of interest None. Funding sources This work was supported by JSPS KAKENHI Grant Number 25860482. References [1] 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. Recommendations of the healthcare infection control practices advisory committee and the HICPAC/SHEA/APIC/IDSA hand hygiene task force. MMWR Recomm Rep 2002;51:1e45. [2] Pratt RJ, Pellowe CM, Wilson JA, Loveday HP, Harper PJ, Jones SR, et al. epic2: national evidence-based guidelines for preventing healthcare-associated infections in NHS hospitals in England. J Hosp Infect 2007;65:S1e64. [3] 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;30:611e22. [4] Guilhermetti M, Marques Wiirzler LA, Castanheira Facio B, da Silva Furlan M, Campo Meschial W, Bronharo Tognim MC, et al. Antimicrobial efficacy of alcohol-based hand gels. J Hosp Infect 2010;74:219e24. [5] Girou E, Loyeau S, Legrand P, Oppein F, Brun-Buisson C. Efficacy of handrubbing with alcohol based solution versus standard handwashing with antiseptic soap: randomised clinical trial. BMJ 2002;325:362e6. [6] Russell AD. Bacterial spores and chemical sporicidal agents. Clin Microbiol Rev 1990;3:99e119. [7] Oughton MT, Loo VG, Dendukuri N, Fenn S, Libman MD. Hand hygiene with soap and water is superior to alcohol rub and antiseptic wipes for removal of Clostridium difficile. Infect Control Hosp Epidemiol 2009;30:939e44. [8] Jabbar U, Leischner J, Kasper D, Gerber R, Sambol SP, Parada JP, et al. Effectiveness of alcohol-based hand rubs for removal of Clostridium difficile spores from hands. Infect Control Hosp Epidemiol 2010;31:565e70. [9] Weber DJ, Sickbert-Bennett E, Gergen MF, Rutala WA. Efficacy of selected hand hygiene agents used to remove Bacillus atrophaeus (a surrogate of Bacillus anthracis) from contaminated hands. JAMA 2003;289:1274e7. [10] Sasahara T, Hayashi S, Hosoda K, Morisawa Y, Hirai Y. Comparison of hand hygiene procedures for removing Bacillus cereus spores. Biocontrol Sci 2014;19:129e34. [11] Freeman J, Bauer MP, Baines SD, Corver J, Fawley WN, Goorhuis B, et al. The changing epidemiology of Clostridium difficile infections. Clin Microbiol Rev 2010;23:529e49. [12] McFarland LV, Mulligan ME, Kwok RY, Stamm WE. Nosocomial acquisition of Clostridium difficile infection. N Engl J Med 1989;320:204e10. [13] Richard V, Van der Auwera P, Snoeck R, Daneau D, Meunier F. Nosocomial bacteremia caused by Bacillus species. Eur J Clin Microbiol Infect Dis 1988;7: 783e5. [14] Matsumoto S, Suenaga H, Naito K, Sawazaki M, Hiramatsu T, Agata N. Management of suspected nosocomial infection: an audit of 19 hospitalized patients with septicemia caused by Bacillus species. Jpn J Infect Dis 2000;53: 196e202.
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