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Staphylococcus aureus surface contamination of mobile phones and presence of genetically identical strains on the hands of nursing personnel
ARTICLE IN PRESS American Journal of Infection Control ■■ (2017) ■■-■■
Contents lists available at ScienceDirect
American Journal of Infection Control
American Journal of Infection Control
j o u r n a l h o m e p a g e : w w w. a j i c j o u r n a l . o r g
Brief Report
Staphylococcus aureus surface contamination of mobile phones and presence of genetically identical strains on the hands of nursing personnel Akiko Katsuse Kanayama PhD a, Hiroshi Takahashi PhD a, Sadako Yoshizawa MD, PhD b, Kazuhiro Tateda MD, PhD c, Akihiro Kaneko DDS, PhD d, Intetsu Kobayashi PhD a,* a
Department of Infection Control and Prevention, Toho University Faculty of Nursing, Tokyo, Japan Department of General Medicine and Emergency Center, Division of Infectious Diseases, Toho University Omori Medical Center, Tokyo, Japan Department of Microbiology and Infectious Diseases, Toho University School of Medicine, Tokyo, Japan d Department of Oral and Maxillofacial Surgery, Tokai University School of Medicine, Kanagawa, Japan b c
Key Words: Staphylococcus aureus DNA fingerprinting Mobile phones Bacterial contamination Health care–associated infection Nursing personnel
We investigated the genetic relatedness of Staphylococcus aureus isolates recovered from mobile phones and palms and fingers of users. Genetically identical isolates were detected from mobile phones and their user and multiple users, which is consistent with mobile phones serving as reservoirs of infection in the health care environment. These findings reinforce the need for hand hygiene prior to patient contact as the most effective intervention for preventing health care–associated infection. © 2016 Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
BACKGROUND
METHODS
In recent years, hospital use–only mobile phones are increasingly used by hospital staff in Japan in delivering medical care. They are one of the most frequently used devices, with one mobile phone assigned to a health care worker during their shift. For this reason, when mobile phones become contaminated with methicillinresistant Staphylococcus aureus (MRSA) and other pathogens, the risk of nosocomial infection spread within the health care facility via the palm or finger of health care personnel is high. Although previous studies have focused on bacterial surface contamination of mobile phones and its potential as a reservoir of infection,1-3 crosscontamination between the device and the palm or fingers of health care personnel has not been adequately studied.1-4 In this study, we investigated the genetic relatedness of bacteria found on mobile phones and bacteria recovered from the palm or fingers of health care personnel.
During the period from August-September 2010, 221 mobile phones and palms and fingers of nursing staff in 23 general wards (wards A-W) of a university hospital were sampled for bacterial contamination. RODAC plates (BD, Tokyo, Japan) were pressed onto the mobile phone keypad. The 5 fingers and palm of 221 users were pressed onto the surface of a CHROMagar Orientation plate (BD). After incubation of plates, cultures were examined for the presence of S aureus. Antimicrobial susceptibility testing was performed by the agar dilution method according to Clinical and Laboratory Standards Institute M100-S21.5 A cefoxitin minimum inhibitory concentration breakpoint of ≥8 μg/mL was used to detect MRSA. Chromosomal DNA was prepared for pulsed-field gel electrophoresis (PFGE) analysis of S aureus as described previously.6 After digestion with Sma I (Takara Bio, Shiga, Japan), DNA fragments were separated by electrophoresis (CHEF-DR II system; Bio-Rad, Tokyo, Japan) at 6 V/cm, with pulse times of 1.0-40 seconds for 18 hours. Fragment patterns were interpreted based on the Tenover criteria.7
* Address correspondence to Intetsu Kobayashi, PhD, Department of Infection Control and Prevention, Toho University Faculty of Nursing, 4-16-20, Omori-Nishi Ota-ku, Tokyo 143-0015, Japan. E-mail address: [email protected] (I. Kobayashi). Funding/support: Supported by the Japan Society for the Promotion of Science (KAKENHI grant no. 22590607). Conflicts of interest: None to report.
RESULTS Of the 221 mobile phones used by nurses, 16 (7.2%) were contaminated with S aureus, of which 5 (2.3%) isolates were MRSA. Of
0196-6553/© 2016 Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ajic.2017.02.011
ARTICLE IN PRESS A. Katsuse Kanayama et al. / American Journal of Infection Control ■■ (2017) ■■-■■
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Fig 1. Pulsed-field gel electrophoresis typing of Staphylococcus aureus recovered from mobile phones (MP) and their users’ hands (H) of 11 nursing staff members. For sample 73, methicillin-resistant S aureus (MRSA) was recovered from the mobile phone, and methicillin-susceptible S aureus (MSSA) was recovered from the hands of the user. For sample 78, MRSA was recovered from the mobile phone, whereas the hands yielded MRSA and MSSA. *MRSA was recovered.
Table 1 Number of Staphylococcus aureus–positive staff members from both user mobile phone and hand
Ward F W D K U P S Others (16 wards) Total
No. of staff members (%)
No. of staff members
S aureus isolated
MRSA isolated
15 9 9 9 9 12 13 145 221
4 (26.7) 2 (22.2) 1 (11.1) 1 (11.1) 1 (11.1) 1 (8.3) 1 (7.7) 0 (0) 11 (5.0)
2* (13.3) 0 (0) 0 (0) 0 (0) 0 (0) 0 (0) 0 (0) 0 (0) 2 (0.9)
MRSA, methicillin-resistant S aureus. *MRSA was isolated from mobile phone and methicillin-susceptible S aureus was from hands of sample 73; MRSA was isolated from mobile phone, and MRSA and methicillin-susceptible S aureus were from hands of sample 78.
the 5 mobile phones contaminated with MRSA, 4 were found in ward F, and 1 was found in ward V. S aureus was isolated from 55 (24.9%) of the 221 nurses’ palm or fingers, of which 13 (5.9%) nurses were positive for MRSA. Of the 23 wards in the hospital, MRSA was detected in the palms or fingers of nurses assigned to 8 wards. The highest isolation rate was found in ward F, where 4 of the 15 MRSA-positive nurses worked. Both the mobile phone and palms or fingers of their user were concurrently S aureus positive in 11 (5.0%) of 221 mobile phone–user paired samplings. Of these 11 paired S aureus–positive samplings, 4 were from ward F (Table 1). For sample 73, MRSA was recovered from the mobile phone and methicillin-susceptible S aureus (MSSA) was recovered from the palms or fingers of the user. For sample 78, MRSA was recovered from the mobile phone, whereas the palm or fingers yielded MRSA and MSSA (Fig 1). Of the 11 S aureus concurrently–positive mobile phone and user pairings, excluding sample 73, the PFGE patterns of the isolates were identical. DISCUSSION The need to rapidly and efficiently manage patients in the hospital environment necessitates frequent use of mobile phones and
other devices. Surface contamination of mobile phones likely occurs when these devices are used with bare hands or gloved hands after contact with a patient. In this study, we performed PFGE analysis of S aureus isolates found on the surfaces of mobile phones and the palm and fingers of nursing personnel. PFGE findings revealed the presence of genetically identical isolates from mobile phones and palms and fingers of nurses consistent with cross-transmission via contaminated mobile phones or palms and fingers. Furthermore, the presence of genetically identical S aureus, including MRSA on mobile phones and palms and fingers of multiple users (data not shown) suggests widespread transmission within the hospital via the palms or fingers of contaminated mobile phone users. Although it is known that hand hygiene is the cornerstone of preventing health care–associated infection,8,9 our data suggest that contact with contaminated mobile phones after handwashing can recontaminate palms or fingers. For this reason, hand hygiene should be repeated after use of mobile phones and prior to patient contact. Even if an effective disinfection method for mobile phones becomes available, such disinfection prior to mobile phone usage is impractical. For this reason, all health care workers should be aware that mobile phones and other devices used in the clinical setting can be a source of hospital-acquired infections and strictly adhere to the World Health Organization guideline on hand hygiene9 prior to patient contact because hygiene is the most effective means of preventing health care–associated infection. References 1. Ulger F, Dilek A, Esen S, Sunbul M, Leblebicioglu H. Are healthcare workers’ mobile phones a potential source of nosocomial infections? Review of the literature. J Infect Dev Ctries 2015;9:1046-53. 2. Brady RR, Verran J, Damani NN, Gibb AP. Review of mobile communication devices as potential reservoirs of nosocomial pathogens. J Hosp Infect 2009;71:295-300. 3. Khan A, Rao A, Reyes-Sacin C, Hayakawa K, Szpunar S, Riederer K, et al. Use of portable electronic devices in a hospital setting and their potential for bacterial colonization. Am J Infect Control 2015;43:286-8. 4. Ulger F, Esen S, Dilek A, Yanik K, Gunaydin M, Leblebicioglu H. Are we aware how contaminated our mobile phones with nosocomial pathogens? Ann Clin Microbiol Antimicrob 2009;8:7. 5. Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing; twenty-first informational supplement. Wayne (PA): Clinical and Laboratory Standards Institute; 2011. M100-S21. 6. Ichiyama S, Ohta M, Shimokata K, Kato N, Takeuchi J. Genomic DNA fingerprinting by pulsed-field gel electrophoresis as an epidemiological marker for study of
ARTICLE IN PRESS A. Katsuse Kanayama et al. / American Journal of Infection Control ■■ (2017) ■■-■■
nosocomial infections caused by methicillin-resistant Staphylococcus aureus. J Clin Microbiol 1991;29:2690-5. 7. Tenover FC, Arbeit RD, Goering RV, Mickelsen PA, Murray BE, Persing DH, et al. Interpreting chromosomal DNA restriction patterns produced by pulsed- field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol 1995; 33:2233-9.
3
8. Song X, Stockwell DC, Floyd T, Short BL, Singh N. Improving hand hygiene compliance in health care workers: strategies and impact on patient outcomes. Am J Infect Control 2013;41:e101-5. 9. World Health Organization. WHO guidelines on hand hygiene in health care. Available from: http://apps.who.int/iris/bitstream/10665/44102/1/9789241597906 _eng.pdf. Accessed February 7, 2017.
Contents lists available at ScienceDirect
American Journal of Infection Control
American Journal of Infection Control
j o u r n a l h o m e p a g e : w w w. a j i c j o u r n a l . o r g
Brief Report
Staphylococcus aureus surface contamination of mobile phones and presence of genetically identical strains on the hands of nursing personnel Akiko Katsuse Kanayama PhD a, Hiroshi Takahashi PhD a, Sadako Yoshizawa MD, PhD b, Kazuhiro Tateda MD, PhD c, Akihiro Kaneko DDS, PhD d, Intetsu Kobayashi PhD a,* a
Department of Infection Control and Prevention, Toho University Faculty of Nursing, Tokyo, Japan Department of General Medicine and Emergency Center, Division of Infectious Diseases, Toho University Omori Medical Center, Tokyo, Japan Department of Microbiology and Infectious Diseases, Toho University School of Medicine, Tokyo, Japan d Department of Oral and Maxillofacial Surgery, Tokai University School of Medicine, Kanagawa, Japan b c
Key Words: Staphylococcus aureus DNA fingerprinting Mobile phones Bacterial contamination Health care–associated infection Nursing personnel
We investigated the genetic relatedness of Staphylococcus aureus isolates recovered from mobile phones and palms and fingers of users. Genetically identical isolates were detected from mobile phones and their user and multiple users, which is consistent with mobile phones serving as reservoirs of infection in the health care environment. These findings reinforce the need for hand hygiene prior to patient contact as the most effective intervention for preventing health care–associated infection. © 2016 Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
BACKGROUND
METHODS
In recent years, hospital use–only mobile phones are increasingly used by hospital staff in Japan in delivering medical care. They are one of the most frequently used devices, with one mobile phone assigned to a health care worker during their shift. For this reason, when mobile phones become contaminated with methicillinresistant Staphylococcus aureus (MRSA) and other pathogens, the risk of nosocomial infection spread within the health care facility via the palm or finger of health care personnel is high. Although previous studies have focused on bacterial surface contamination of mobile phones and its potential as a reservoir of infection,1-3 crosscontamination between the device and the palm or fingers of health care personnel has not been adequately studied.1-4 In this study, we investigated the genetic relatedness of bacteria found on mobile phones and bacteria recovered from the palm or fingers of health care personnel.
During the period from August-September 2010, 221 mobile phones and palms and fingers of nursing staff in 23 general wards (wards A-W) of a university hospital were sampled for bacterial contamination. RODAC plates (BD, Tokyo, Japan) were pressed onto the mobile phone keypad. The 5 fingers and palm of 221 users were pressed onto the surface of a CHROMagar Orientation plate (BD). After incubation of plates, cultures were examined for the presence of S aureus. Antimicrobial susceptibility testing was performed by the agar dilution method according to Clinical and Laboratory Standards Institute M100-S21.5 A cefoxitin minimum inhibitory concentration breakpoint of ≥8 μg/mL was used to detect MRSA. Chromosomal DNA was prepared for pulsed-field gel electrophoresis (PFGE) analysis of S aureus as described previously.6 After digestion with Sma I (Takara Bio, Shiga, Japan), DNA fragments were separated by electrophoresis (CHEF-DR II system; Bio-Rad, Tokyo, Japan) at 6 V/cm, with pulse times of 1.0-40 seconds for 18 hours. Fragment patterns were interpreted based on the Tenover criteria.7
* Address correspondence to Intetsu Kobayashi, PhD, Department of Infection Control and Prevention, Toho University Faculty of Nursing, 4-16-20, Omori-Nishi Ota-ku, Tokyo 143-0015, Japan. E-mail address: [email protected] (I. Kobayashi). Funding/support: Supported by the Japan Society for the Promotion of Science (KAKENHI grant no. 22590607). Conflicts of interest: None to report.
RESULTS Of the 221 mobile phones used by nurses, 16 (7.2%) were contaminated with S aureus, of which 5 (2.3%) isolates were MRSA. Of
0196-6553/© 2016 Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ajic.2017.02.011
ARTICLE IN PRESS A. Katsuse Kanayama et al. / American Journal of Infection Control ■■ (2017) ■■-■■
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Fig 1. Pulsed-field gel electrophoresis typing of Staphylococcus aureus recovered from mobile phones (MP) and their users’ hands (H) of 11 nursing staff members. For sample 73, methicillin-resistant S aureus (MRSA) was recovered from the mobile phone, and methicillin-susceptible S aureus (MSSA) was recovered from the hands of the user. For sample 78, MRSA was recovered from the mobile phone, whereas the hands yielded MRSA and MSSA. *MRSA was recovered.
Table 1 Number of Staphylococcus aureus–positive staff members from both user mobile phone and hand
Ward F W D K U P S Others (16 wards) Total
No. of staff members (%)
No. of staff members
S aureus isolated
MRSA isolated
15 9 9 9 9 12 13 145 221
4 (26.7) 2 (22.2) 1 (11.1) 1 (11.1) 1 (11.1) 1 (8.3) 1 (7.7) 0 (0) 11 (5.0)
2* (13.3) 0 (0) 0 (0) 0 (0) 0 (0) 0 (0) 0 (0) 0 (0) 2 (0.9)
MRSA, methicillin-resistant S aureus. *MRSA was isolated from mobile phone and methicillin-susceptible S aureus was from hands of sample 73; MRSA was isolated from mobile phone, and MRSA and methicillin-susceptible S aureus were from hands of sample 78.
the 5 mobile phones contaminated with MRSA, 4 were found in ward F, and 1 was found in ward V. S aureus was isolated from 55 (24.9%) of the 221 nurses’ palm or fingers, of which 13 (5.9%) nurses were positive for MRSA. Of the 23 wards in the hospital, MRSA was detected in the palms or fingers of nurses assigned to 8 wards. The highest isolation rate was found in ward F, where 4 of the 15 MRSA-positive nurses worked. Both the mobile phone and palms or fingers of their user were concurrently S aureus positive in 11 (5.0%) of 221 mobile phone–user paired samplings. Of these 11 paired S aureus–positive samplings, 4 were from ward F (Table 1). For sample 73, MRSA was recovered from the mobile phone and methicillin-susceptible S aureus (MSSA) was recovered from the palms or fingers of the user. For sample 78, MRSA was recovered from the mobile phone, whereas the palm or fingers yielded MRSA and MSSA (Fig 1). Of the 11 S aureus concurrently–positive mobile phone and user pairings, excluding sample 73, the PFGE patterns of the isolates were identical. DISCUSSION The need to rapidly and efficiently manage patients in the hospital environment necessitates frequent use of mobile phones and
other devices. Surface contamination of mobile phones likely occurs when these devices are used with bare hands or gloved hands after contact with a patient. In this study, we performed PFGE analysis of S aureus isolates found on the surfaces of mobile phones and the palm and fingers of nursing personnel. PFGE findings revealed the presence of genetically identical isolates from mobile phones and palms and fingers of nurses consistent with cross-transmission via contaminated mobile phones or palms and fingers. Furthermore, the presence of genetically identical S aureus, including MRSA on mobile phones and palms and fingers of multiple users (data not shown) suggests widespread transmission within the hospital via the palms or fingers of contaminated mobile phone users. Although it is known that hand hygiene is the cornerstone of preventing health care–associated infection,8,9 our data suggest that contact with contaminated mobile phones after handwashing can recontaminate palms or fingers. For this reason, hand hygiene should be repeated after use of mobile phones and prior to patient contact. Even if an effective disinfection method for mobile phones becomes available, such disinfection prior to mobile phone usage is impractical. For this reason, all health care workers should be aware that mobile phones and other devices used in the clinical setting can be a source of hospital-acquired infections and strictly adhere to the World Health Organization guideline on hand hygiene9 prior to patient contact because hygiene is the most effective means of preventing health care–associated infection. References 1. Ulger F, Dilek A, Esen S, Sunbul M, Leblebicioglu H. Are healthcare workers’ mobile phones a potential source of nosocomial infections? Review of the literature. J Infect Dev Ctries 2015;9:1046-53. 2. Brady RR, Verran J, Damani NN, Gibb AP. Review of mobile communication devices as potential reservoirs of nosocomial pathogens. J Hosp Infect 2009;71:295-300. 3. Khan A, Rao A, Reyes-Sacin C, Hayakawa K, Szpunar S, Riederer K, et al. Use of portable electronic devices in a hospital setting and their potential for bacterial colonization. Am J Infect Control 2015;43:286-8. 4. Ulger F, Esen S, Dilek A, Yanik K, Gunaydin M, Leblebicioglu H. Are we aware how contaminated our mobile phones with nosocomial pathogens? Ann Clin Microbiol Antimicrob 2009;8:7. 5. Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing; twenty-first informational supplement. Wayne (PA): Clinical and Laboratory Standards Institute; 2011. M100-S21. 6. Ichiyama S, Ohta M, Shimokata K, Kato N, Takeuchi J. Genomic DNA fingerprinting by pulsed-field gel electrophoresis as an epidemiological marker for study of
ARTICLE IN PRESS A. Katsuse Kanayama et al. / American Journal of Infection Control ■■ (2017) ■■-■■
nosocomial infections caused by methicillin-resistant Staphylococcus aureus. J Clin Microbiol 1991;29:2690-5. 7. Tenover FC, Arbeit RD, Goering RV, Mickelsen PA, Murray BE, Persing DH, et al. Interpreting chromosomal DNA restriction patterns produced by pulsed- field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol 1995; 33:2233-9.
3
8. Song X, Stockwell DC, Floyd T, Short BL, Singh N. Improving hand hygiene compliance in health care workers: strategies and impact on patient outcomes. Am J Infect Control 2013;41:e101-5. 9. World Health Organization. WHO guidelines on hand hygiene in health care. Available from: http://apps.who.int/iris/bitstream/10665/44102/1/9789241597906 _eng.pdf. Accessed February 7, 2017.