225 C OPYRIGHT Ó 2015
BY
T HE J OURNAL
OF
B ONE
AND J OINT
S URGERY, I NCORPORATED
Investigation of Cell Phones as a Potential Source of Bacterial Contamination in the Operating Room Irshad A. Shakir, MD, Nirav H. Patel, MD, Robin R. Chamberland, PhD, and Scott G. Kaar, MD Investigation performed at the Department of Orthopaedic Surgery, Saint Louis University, St. Louis, Missouri
Background: Cell phone use has become common in areas of the hospital, including the operating room. The purpose of this study was to document the frequency of bacterial contamination on the cell phones of orthopaedic surgeons in the operating room and to determine whether a standardized disinfecting protocol decreased the rate of bacterial contamination and the amount of organic material. Methods: Orthopaedic attending and resident cell phones were swabbed on the front and back in the operating room with adenosine triphosphate bioluminescence to quantify organic material contamination and culture swabs to evaluate bacterial contamination. Adenosine triphosphate was quantified with use of relative light units. One photon of light was emitted for each molecule of adenosine triphosphate. Thresholds of 250 and 500 relative light units were used. The phones were cleaned with a cleaning wipe and were retested. One week later, a final set of studies was obtained. Fifty-three participants were enrolled in this study. Pathogenic bacteria were defined as those commonly causing surgical site infections. Results: Of fifty-three cell phones, 83% (forty-four cell phones) had pathogenic bacteria at initial testing, 8% (four cell phones) had pathogenic bacteria after disinfection, and 75% (forty cell phones) had pathogenic bacteria one week later. The mean result (and standard deviation) at initial testing was 3488 ± 2998 relative light units, which reduced after disinfection to 200 ± 123 relative light units, indicating a cleaned surface, but increased one week later to 1825 ± 1699 relative light units, indicating a poorly cleaned surface. Conclusions: The cell phones of orthopaedic surgeons had a high rate of pathogenic bacteria and organic material contamination. Both were decreased after a single disinfecting process. However, recontamination occurred. It seems prudent to routinely disinfect them or avoid their use in the operating room. Clinical Relevance: The current study investigates orthopaedic surgeons’ cell phones as a potential source of nosocomial infection in the operating room. On the basis of the high percentage of cell phone contamination found, we would recommend periodic cell phone cleaning with either the wipes used in our study or similar ones. In addition, given that there was a high contamination rate one week after disinfection, we would recommend considering cell phone cleaning more frequently than once a week.
Peer Review: This article was reviewed by the Editor-in-Chief and one Deputy Editor, and it underwent blinded review by two or more outside experts. It was also reviewed by an expert in methodology and statistics. The Deputy Editor reviewed each revision of the article, and it underwent a final review by the Editor-in-Chief prior to publication. Final corrections and clarifications occurred during one or more exchanges between the author(s) and copyeditors.
T
he cell phones used in hospitals may serve as vehicles for nosocomial transmission of microorganisms1,2. Bacterial contamination is present in about 95% of the cell phones of hospital workers, and 14.3% of cell phones were contaminated with bacteria that can cause nosocomial infection1-3. The cell phones of health-care workers are potential vectors
for transferring nosocomial pathogens among health-care workers, patients, and the community4. Cell phones are challenging to disinfect without damaging the device. Apple (Cupertino, California) and Samsung (Samsung Town, Seoul, South Korea) recommend cleaning their devices with a lint-free cloth, yet it is rarely done5,6. We are aware of no
Disclosure: None of the authors received payments or services, either directly or indirectly (i.e., via his or her institution), from a third party in support of any aspect of this work. None of the authors, or their institution(s), have had any financial relationship, in the thirty-six months prior to submission of this work, with any entity in the biomedical arena that could be perceived to influence or have the potential to influence what is written in this work. Also, no author has had any other relationships, or has engaged in any other activities, that could be perceived to influence or have the potential to influence what is written in this work. The complete Disclosures of Potential Conflicts of Interest submitted by authors are always provided with the online version of the article.
J Bone Joint Surg Am. 2015;97:225-31
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http://dx.doi.org/10.2106/JBJS.N.00523
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TABLE I Bacteria Divided on the Basis of the Culture Results Pathogenic Bacteria
Nonpathogenic Bacteria
Coagulase-negative staphylococci
Bacillus species
Viridans streptococci
Micrococcus species
Staphylococcus aureus
Corynebacterium species
Enterococcus faecalis
Lactobacillus species Paracoccus yeei Pseudomonas oryzihabitans
universally accepted guidelines for the disinfection of cell phones. The efficacy of sterilization can be defined as whether repeat cultures are positive after disinfecting the tested surface. Alternative studies have examined the use of adenosine triphosphate (ATP) bioluminescence to monitor the efficacy7-13. One study examined how effective decontamination was in the operating room using this system14. ATP is present in a wide variety of organic material, such as bacteria, food, and human secretions and excretions, and has been used in the food and beverage industries to assess the adequacy of cleaning procedures8,15. This surfaceswabbing technique involved a reaction of ATP with luciferin and luciferase enzyme, resulting in the emission of light. This light was then detected with use of a handheld luminometer, giving a result in only a few seconds10. A threshold between 250 and 500 relative light units indicated a clean surface12, whereas poorly cleaned surfaces yielded >1000 relative light units13. Willis et al. concluded that ATP bioluminescence was not directly equivalent to microbiological testing but was a useful tool for monitoring cleanliness10. This study investigated the presence of bacteria on cell phones in an orthopaedic operating room and the efficacy of recommended cleaning methods. Our hypothesis was that cell phones are a potential source for bacterial contamination and that a standardized disinfecting protocol would substantially decrease their rate of bacterial contamination and the amount of organic material present. We also hypothesized that the likelihood of a positive culture and the amount of organic material will remain decreased one week after disinfecting. Materials and Methods
A
fter approval from the institutional review board, the study was performed at the five operating room sites affiliated with our institution. The study enrolled all attending and resident orthopaedic surgeons at our university-based program for a total of fifty-three participants.
CELL PHON ES AS A POTEN TIA L SOU RCE OF BACTER IA L C O N TA M I N AT I O N I N T H E O P E R AT I N G R O O M
an overlapping “S” pattern was used to cover the entire surface with horizontal strokes with a rolling motion to maximize contact with the surface. Then the same area was swabbed again using vertical “S” strokes, and finally the swab was rotated once more using diagonal “S” strokes (see Appendix) in accordance with 16 similar recommendations from the Centers for Disease Control and Prevention . These right-sided samples were placed into ATP bioluminescence re13 action tubes and were agitated for at least five seconds . The relative light units were immediately measured on the Clean-Trace Luminometers. Relative light units are measured because one photon of light is emitted for each molecule of ATP present. The left-sided samples were cultured on 5% sheep blood agar (BBL; Becton Dickinson, Sparks, Maryland) incubated at 37°C in 5% CO2 and MacConkey agar incubated at 37°C in air. Plates were examined at twenty-four and forty-eight hours, and all colony types present were subjected to Gram stain and biochemical identification. Identification was performed with use of catalase reagent (H2O2), Staphaurex (Remel, Lenexa, Kansas), and Vitek 2 (bioM´erieux, Durham, North Carolina). Susceptibility testing was performed on organisms deemed clinically meaningful with use of Vitek 2. Antimicrobials tested were based on those that would be reported for organisms in a surgical 17,18 site infection .
Cleaning Regimen and Survey The cell phones underwent a standardized disinfecting protocol with Bausch & Lomb Clens wipes (Rochester, New York). These wipes were labeled as safe for Apple products and were used for all phones because of their low concentration of alcohol to disinfect without damaging. Because all cell phones were individually owned, we chose a product that was endorsed by the manufacturer so that it would not void any warranty or damage the product. The main ingredient is 32% isopropyl alcohol and a proprietary protected detergent. The disinfecting technique was identical to the swab technique to cleanse the entire surface area of the device. After a standardized time of five minutes, which was used so that any and all residual products were not present on the sampled surface, the cell phone was tested again with use of the same technique for repeat cultures and ATP bioluminescence. During the wait time, a verbal questionnaire was given to all participants in the study on the extent of usage of their cell phones, the locations of use, the use of headsets, the awareness of disinfection practices of cell phones, and the frequency of hand-washing after 19 using their phones . One week later, all phones were then retested by swabbing for cultures and ATP bioluminescence. A second questionnaire was then given regarding whether or not their cleaning practices had changed. The bacterial growth results were further divided into pathogenic and nonpathogenic bacteria on the basis of the organisms recovered. Other common bacteria that did not grow from culture specimens from the study participants’ cell phones were omitted. These organisms were divided by those most likely to cause surgical site infection according to the Guide to the Elimination of Orthopedic Surgical Site Infections by the Association for Professionals 17,18 in Infection Control and Epidemiology (APIC) (Table I) . The ATP results were then further classified as 500 relative light units and 250 relative light units on the basis of the previously discussed ATP benchmarks, in which the threshold between 250 and 12,13 500 relative light units indicated a clean surface .
TABLE II Relative Light Units and Culture Results at Each Time Point
Sampling Protocol Each cell phone was tested, on both the front and back surfaces, in the operating room while the surgeon was scrubbed into surgery. The phone was placed on a sterile towel during testing and was handled with sterile gloves to minimize the risk of contamination. The phone was divided in half from top to bottom. The left side of the phone was swabbed for inoculation on blood and MacConkey agar and was labeled with a randomized number and a letter: A for initial, B for after disinfection, and C for one week later. The right side was swabbed for ATP bioluminescence assay (3M Clean-Trace Surface ATP; 3M, St. Paul, Minnesota). The technique was standardized and was labeled in a similar fashion. First,
Bacteria Grown on Culture Time Point Initial After disinfection One week later
Relative Light Units*
Pathogenic
Nonpathogenic
3488 ± 2998
83%
59%
200 ± 123
8%
9%
1825 ± 1699
75%
30%
*The values are given as the mean and the standard deviation.
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CELL PHON ES AS A POTEN TIA L SOU RCE OF BACTER IA L C O N TA M I N AT I O N I N T H E O P E R AT I N G R O O M
TABLE III Culture Results Based on the Type of Bacteria at Each Time Point Time Point Initial After disinfection One week later
Coagulase-Negative Staphylococci*
Viridans Streptococci*
Staphylococcus Aureus*
Enterococcus Faecalis*
40
2
4
0
6
0
1
0
39
2
4
1
*The values are given as the number of phones with positive results.
Study Population The study group consisted of fifty-three participants (forty-one male participants and twelve female participants), and there were twenty attending physicians and thirty-three residents. There were three brands of phones tested: forty-four Apple, eight Samsung, and one Blackberry (Waterloo, Ontario, Canada). There were ten different models among these manufacturers. Thirtynine of the fifty-three participants had cases on their phones, and, of those, twenty-six had “smooth” cases with no grooves or crevices and thirteen had “rough” cases with grooves or crevices. The phones were divided into three groups based on size. Size was defined as the average being the size of an iPhone 5, 5c, or 5s (Apple) (twenty-seven of fifty-three phones), which was 4.9 inches (12.5 cm) long. One group was this average size at 4.9 inches (12.5 cm), the second group was smaller than the average size at 12.5 cm).
Statistics Our primary measures were bacterial growths on culture and mean relative light units on cell phones on initial presentation. Our secondary outcome 13 measures were determination of the difference before and after cleaning . Continuous data were analyzed with use of either the paired or Student t test. The Pearson chi-square test was used for nominal data along with relative risk and its 95% confidence intervals for cutoff values of 250 and 500 relative light units and pathogenic growth. The Fisher exact test was used for analyses of categorical variables with small expected cell frequencies. Two-sided signifi-
cance was set at p < 0.05. We used a convenience sample without sample-sized calculations. Therefore, some of the analyses of predictors of contamination may be underpowered.
Source of Funding There was no source of external funding for this study.
Results he mean results (and standard deviation) were 3488 ± 2998 relative light units at the initial swab, 200 ± 123 relative light units after disinfection, and 1825 ± 1699 relative light units one week following disinfection (Table II and Fig. 1). Of the fifty-three participants who had >500 relative light units, there were fifty-two (98%) at the initial swab, one (2%) after disinfection, and forty-eight (91%) one week later. Of the fiftythree participants who had >250 relative light units, there were fifty-two (98%) at the initial swab, nine (17%) after disinfection, and fifty-one (96%) one week later. Culture specimens were taken for all fifty-three cell phones. Pathogenic bacteria grew on forty-four cultures (83%) and nonpathogenic bacteria grew on thirty-one cultures (59%) on initial swab; pathogenic bacteria grew on four cultures (8%)
T
Fig. 1
ATP mean results in relative light units (RLUs) at each time point: initial swab, after disinfection, and one week later. SD = standard deviation.
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TABLE IV Initial and One-Week Survey Questions with Results Questions
Front only
Results
2%
Front and back (snap-in with soft screen protector)
21%
4%
Complete (e.g., LifeProof)
38%
8%
Back only
40%
Texting Calling
49% 28%
Internet E-mailing
11%
What is the daily frequency of your usage? Two to five times
Questions What kind of case does your phone have?
What is the phone used for?
Once
TABLE IV (continued)
Results
Initial survey data
All
CELL PHON ES AS A POTEN TIA L SOU RCE OF BACTER IA L C O N TA M I N AT I O N I N T H E O P E R AT I N G R O O M
0%
One-week survey data Have you changed your phone-cleaning practices?
5%
Yes
13%
Six to twenty times Twenty-one to fifty times
21% 53%
No
87%
More than fifty times
21%
How often is the phone cleaned now? Never
19%
Home
9%
After every use After one to five uses
Car
0%
After six to ten uses
Gym
4%
Once a week
30%
Every couple of weeks
21%
Where is the phone most commonly used?
Hospital Where is the phone used in the hospital? Office Outside patient’s room
87% 38% 38%
Emergency room
4%
Operating room
9%
On-call room
11%
Yes No Do you know the manufacturer’s cleaning technique?
42% 58%
Yes
2%
No
98%
Do you know the hospital’s cleaning recommendations? Yes No
0% 100%
How often do you clean your hands after phone use? Never After every use
47% 0%
After two to five uses After six to ten uses
13% 4%
After every patient seen
36%
How often is the phone cleaned? Never After every use
26% 0%
After two to five uses
4%
After six to ten uses
19%
Once a week Every couple of weeks
15% 36%
continued
30%
How often do you clean your hands after phone use? Never After every use
0% 0%
After two to five uses
8%
After six to ten uses
8%
After every patient seen
Does the phone have hands-free Bluetooth?
0% 0%
84%
Have you changed your hand-washing practice? Yes No
17% 83%
and nonpathogenic bacteria grew on five cultures (9%) after disinfection; and pathogenic bacteria grew on forty cultures (75%) and nonpathogenic bacteria grew on sixteen cultures (30%) one week later. For the focus of this study, we concentrated on only pathogenic bacteria in relation to relative light units (Table III and Fig. 2). Staphylococcus aureus was identified on four cell phones both before screening and one week later but was only identified on one phone after disinfecting initially. Comparing relative light units of 500 with whether the phone grew pathogenic bacteria on culture demonstrated significance (p = 0.03) at the initial swab, but not after disinfection, and it was nearly significant (p = 0.053) one week later (see Appendix). This is consistent with expectations that, as relative light units exceed 500, there would be an increased amount of pathogenic bacterial growth as demonstrated by samples initially and one week later. Comparing relative light units of 250 with pathogenic bacterial growth on culture demonstrated significance at the initial swab but not after disinfection or after one week (see Appendix). Although forty-six (87%) of fifty-three phones had a decrease in the relative light units one week after disinfection by more than half, 75% had cultures positive for pathogenic bacteria.
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CELL PHON ES AS A POTEN TIA L SOU RCE OF BACTER IA L C O N TA M I N AT I O N I N T H E O P E R AT I N G R O O M
Fig. 2
Percentage of pathogenic and nonpathogenic bacterial results at each time point: initial swab, after disinfection, and one week later.
When looking at relative light units and bacterial growth, there was no significant difference between male and female sex (p = 0.59), between attending physicians’ cell phones and residents’ cell phones (p = 0.20), between cell phones with a case and those without a case (p = 0.11), between a smooth case and a rough case (p = 0.17), or among the three sizes of the cell phones in this study (p = 0.73) (see Appendix). Table IV demonstrates the initial and one-week survey results. On the initial survey, almost half of the physicians used their phones for texting approximately twenty-one to fifty times a day. Expectedly, most of the use was at the hospital and nearly all participants did not know what the cleaning recommendation was for their phones. Of the fifty-three participants in this study, 36% (nineteen participants) cleaned their phones every couple of weeks and 40% (twenty-one participants) had back-only cases on their phones. One week later, 87% (forty-six participants) had changed their phone-cleaning practices. Thirty percent (sixteen participants) increased their cleaning to after six to ten uses up from 19% (ten participants) before the study. Of the fifty-three participants, 30% (sixteen participants) increased their cleaning to once a week up from 15% (eight participants) before the study. Discussion e believe this to be the first study to investigate cell phones as a potential source of bacterial contamination in the operating room using both relative light units and cultures. We demonstrated that cell phones had a contamination rate of 83% (forty-four participants) based on cultures, similar to, but not as high as, previous studies2,3. On the basis of relative light units, 98% (fifty-two participants) of phones had a value greater than what is considered clean. Prior studies used various relative light unit targets ranging from 250 to 500, which have been shown to
W
indicate decreased bacterial colony counts on various inpatient care surfaces. This has been linked to incremental quality improvements13. There was a noticeable decrease in relative light units and amount of bacterial growth on culture after a simple cleanse of the phone. This small effort decreased ATP and the likelihood of pathogenic-positive cultures. A recent prevalence study found that surgical site infections were the most common health care-associated infection, accounting for 31% of all hospital-acquired infections among hospitalized patients20. The National Healthcare Safety Network data for 2006 to 2008 showed an overall surgical site infection rate of 1.9% with 16,147 surgical site infections following 849,659 operative procedures21. It is yet unknown whether there is a correlation of cell phone contamination with surgical site infection rates and/or bacteria found in surgical site infections. A weakness of our study was that we did not follow each patient to determine whether a surgical site infection developed. Therefore, no official recommendations can be made regarding cell phone use or disinfection in operating rooms. However, it seems reasonable to recommend that a surgeon disinfect his or her phone as a precautionary measure if it is going to be used in the operating room. A limitation of our study was the inability to answer the question of whether the products in the wipe itself impacted the sampling results or if the mechanical act of wiping alone would have been sufficient. Another limitation of our study was that we did not quantify bacterial growth in number of colonies. This was intended to answer the question of what is growing on cell phones of orthopaedic surgeons and not how many colonies were growing. Additional studies could quantify the number of colonies and determine if there is a correlation between the number of colonies and the number of relative light units. Additional studies could
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also evaluate the efficacy of ultraviolet light for the decontamination of cell phones. Willis et al. demonstrated inconsistent correlation between relative light unit count and positive growth on culture and concluded that ATP bioluminescence is not directly correlated to cultures; however, the instant results support its use as a beneficial tool for monitoring cleanliness10. It is also important to note that bacterial cultures do not assess for other biological contaminants such as viruses or eukaryotic cells, whereas the ATP luminometer does. One review article pooled data on mobile communication devices and, with regard to device cleaning, recommended restricting the use of cell phone technology in certain high-risk areas, such as operating rooms, intensive care units, and burn units22. In another recent study, Beckstrom et al. reviewed bacterial contamination of parents’ cell phones in a neonatal intensive care unit and the effectiveness of an anti-microbial gel in reducing transmission to the hands23. They demonstrated that all cell phones had bacterial contamination and 90% had the same bacteria on the cell phone and on the parents’ hands23. This demonstrates the need for proper hand-washing techniques as well as the importance of cell phone cleanliness because only disinfecting one or the other results in continued contamination of both. In conclusion, cell phones of orthopaedic surgeons are used commonly in the operating room and we found a high rate of pathogenic bacterial contamination and organic material on them. This bacterial and organic material load was decreased after a single disinfecting process with commercially available cleaning wipes safe for cell phone use. One week after disinfection, a cell phone had a high likelihood of bacterial recontamination, although the amount of accumulated organic material was decreased compared with that before disinfection. Although the risk that cell phones pose as a source of surgical site infections is yet unknown, to our knowledge, it seems
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prudent for surgeons who use their cell phones in the operating room to regularly disinfect them or to consider not using them at all in the operating room. Appendix A figure demonstrating the swabbing technique used on each phone for both ATP and bacterial cultures and tables showing a comparison of dichotomized pathogen counts at the three time points and demographic data are available with the online version of this article as a data supplement at jbjs.org. n NOTE: We especially thank Dr. Heidi Israel, PhD in statistics, for her help in analyzing the data. We also thank Dr. Berton R. Moed, chairman of the Department of Orthopaedic Surgery, for his expertise, guidance, and support on this project.
Irshad A. Shakir, MD Scott G. Kaar, MD Department of Orthopaedic Surgery, Saint Louis University, 3635 Vista Avenue, Desloge Towers, 7th Floor, St. Louis, MO 63110. E-mail address for S.G. Karr: [email protected] Nirav H. Patel, MD Department of Internal Medicine, Division of Infectious Diseases, Saint Louis University, 3635 Vista at Grand Boulevard, St. Louis, MO 63110 Robin R. Chamberland, PhD Department of Pathology, Saint Louis University, 1402 South Grand Boulevard, St. Louis, MO 63104
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10. Willis C, Morley R, Westbury J, Greenwood M, Pallett A. Evaluation of ATP bioluminescence swabbing as a monitoring and training tool for effective hospital cleaning. Br J Infect Control. 2007;8:17-21. 11. Sherlock O, O’Connell N, Creamer E, Humphreys H. Is it really clean? An evaluation of the efficacy of four methods for determining hospital cleanliness. J Hosp Infect. 2009 Jun;72(2):140-6. Epub 2009 Mar 24. 12. Lewis T, Griffith C, Gallo M, Weinbren M. A modified ATP benchmark for evaluating the cleaning of some hospital environmental surfaces. J Hosp Infect. 2008 Jun;69(2):156-63. Epub 2008 May 12. 13. Boyce JM, Havill NL, Dumigan DG, Golebiewski M, Balogun O, Rizvani R. Monitoring the effectiveness of hospital cleaning practices by use of an adenosine triphosphate bioluminescence assay. Infect Control Hosp Epidemiol. 2009 Jul;30 (7):678-84. 14. Vande Leest L, Kawczynski R, Esser Lipp F, Barrientos R. Identifying potential areas of infectivity on high-touch locations in the OR. AORN J. 2012 Nov;96(5):507-12. 15. Davidson CA, Griffith CJ, Peters AC, Fielding LM. Evaluation of two methods for monitoring surface cleanliness-ATP bioluminescence and traditional hygiene swabbing. Luminescence. 1999 Jan-Feb;14(1):33-8. 16. Centers for Disease Control and Prevention. Emergency response resources: Surface sampling procedures for Bacillus anthracis spores from smooth, non-porous surfaces. 2012. http://www.cdc.gov/niosh/topics/emres/surface-samplingbacillus-anthracis.html. Accessed 2014 Feb 17. 17. Greene LR. Guide to the elimination of orthopedic surgery surgical site infections: an executive summary of the Association for Professionals in Infection Control
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and Epidemiology elimination guide. Am J Infect Control. 2012 May;40(4):384-6. Epub 2011 Aug 25. 18. Greene LR, Mills R, Moss R. Association for Professionals in Infection Control and Epidemiology. Guide to the elimination of orthopedic surgical site infections. 2010. http://www.apic.org/Resource_/EliminationGuideForm/34e03612-d1e64214-a76b-e532c6fc3898/File/APIC-Ortho-Guide.pdf. Accessed 2014 Oct 3. 19. Ramesh J, Carter AO, Campbell MH, Gibbons N, Powlett C, Moseley H Sr, Lewis D, Carter T. Use of mobile phones by medical staff at Queen Elizabeth Hospital, Barbados: evidence for both benefit and harm. J Hosp Infect. 2008 Oct;70(2):160-5. Epub 2008 Aug 12. 20. Magill SS, Hellinger W, Cohen J, Kay R, Bailey C, Boland B, Carey D, de Guzman J, Dominguez K, Edwards J, Goraczewski L, Horan T, Miller M, Phelps M, Saltford R, Seibert J, Smith B, Starling P, Viergutz B, Walsh K, Rathore M, Guzman N,
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Fridkin S. Prevalence of healthcare-associated infections in acute care hospitals in Jacksonville, Florida. Infect Control Hosp Epidemiol. 2012 Mar;33(3):283-91. Epub 2012 Jan 12. 21. Mu Y, Edwards JR, Horan TC, Berrios-Torres SI, Fridkin SK. Improving riskadjusted measures of surgical site infection for the National Healthcare Safety Network. Infect Control Hosp Epidemiol. 2011 Oct;32(10):970-86. Epub 2011 Sep 1. 22. Brady RR, Verran J, Damani NN, Gibb AP. Review of mobile communication devices as potential reservoirs of nosocomial pathogens. J Hosp Infect. 2009 Apr;71(4):295-300. Epub 2009 Jan 24. 23. Beckstrom AC, Cleman PE, Cassis-Ghavami FL, Kamitsuka MD. Surveillance study of bacterial contamination of the parent’s cell phone in the NICU and the effectiveness of an anti-microbial gel in reducing transmission to the hands. J Perinatol. 2013 Dec;33(12):960-3. Epub 2013 Sep 5.
BY
T HE J OURNAL
OF
B ONE
AND J OINT
S URGERY, I NCORPORATED
Investigation of Cell Phones as a Potential Source of Bacterial Contamination in the Operating Room Irshad A. Shakir, MD, Nirav H. Patel, MD, Robin R. Chamberland, PhD, and Scott G. Kaar, MD Investigation performed at the Department of Orthopaedic Surgery, Saint Louis University, St. Louis, Missouri
Background: Cell phone use has become common in areas of the hospital, including the operating room. The purpose of this study was to document the frequency of bacterial contamination on the cell phones of orthopaedic surgeons in the operating room and to determine whether a standardized disinfecting protocol decreased the rate of bacterial contamination and the amount of organic material. Methods: Orthopaedic attending and resident cell phones were swabbed on the front and back in the operating room with adenosine triphosphate bioluminescence to quantify organic material contamination and culture swabs to evaluate bacterial contamination. Adenosine triphosphate was quantified with use of relative light units. One photon of light was emitted for each molecule of adenosine triphosphate. Thresholds of 250 and 500 relative light units were used. The phones were cleaned with a cleaning wipe and were retested. One week later, a final set of studies was obtained. Fifty-three participants were enrolled in this study. Pathogenic bacteria were defined as those commonly causing surgical site infections. Results: Of fifty-three cell phones, 83% (forty-four cell phones) had pathogenic bacteria at initial testing, 8% (four cell phones) had pathogenic bacteria after disinfection, and 75% (forty cell phones) had pathogenic bacteria one week later. The mean result (and standard deviation) at initial testing was 3488 ± 2998 relative light units, which reduced after disinfection to 200 ± 123 relative light units, indicating a cleaned surface, but increased one week later to 1825 ± 1699 relative light units, indicating a poorly cleaned surface. Conclusions: The cell phones of orthopaedic surgeons had a high rate of pathogenic bacteria and organic material contamination. Both were decreased after a single disinfecting process. However, recontamination occurred. It seems prudent to routinely disinfect them or avoid their use in the operating room. Clinical Relevance: The current study investigates orthopaedic surgeons’ cell phones as a potential source of nosocomial infection in the operating room. On the basis of the high percentage of cell phone contamination found, we would recommend periodic cell phone cleaning with either the wipes used in our study or similar ones. In addition, given that there was a high contamination rate one week after disinfection, we would recommend considering cell phone cleaning more frequently than once a week.
Peer Review: This article was reviewed by the Editor-in-Chief and one Deputy Editor, and it underwent blinded review by two or more outside experts. It was also reviewed by an expert in methodology and statistics. The Deputy Editor reviewed each revision of the article, and it underwent a final review by the Editor-in-Chief prior to publication. Final corrections and clarifications occurred during one or more exchanges between the author(s) and copyeditors.
T
he cell phones used in hospitals may serve as vehicles for nosocomial transmission of microorganisms1,2. Bacterial contamination is present in about 95% of the cell phones of hospital workers, and 14.3% of cell phones were contaminated with bacteria that can cause nosocomial infection1-3. The cell phones of health-care workers are potential vectors
for transferring nosocomial pathogens among health-care workers, patients, and the community4. Cell phones are challenging to disinfect without damaging the device. Apple (Cupertino, California) and Samsung (Samsung Town, Seoul, South Korea) recommend cleaning their devices with a lint-free cloth, yet it is rarely done5,6. We are aware of no
Disclosure: None of the authors received payments or services, either directly or indirectly (i.e., via his or her institution), from a third party in support of any aspect of this work. None of the authors, or their institution(s), have had any financial relationship, in the thirty-six months prior to submission of this work, with any entity in the biomedical arena that could be perceived to influence or have the potential to influence what is written in this work. Also, no author has had any other relationships, or has engaged in any other activities, that could be perceived to influence or have the potential to influence what is written in this work. The complete Disclosures of Potential Conflicts of Interest submitted by authors are always provided with the online version of the article.
J Bone Joint Surg Am. 2015;97:225-31
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http://dx.doi.org/10.2106/JBJS.N.00523
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TABLE I Bacteria Divided on the Basis of the Culture Results Pathogenic Bacteria
Nonpathogenic Bacteria
Coagulase-negative staphylococci
Bacillus species
Viridans streptococci
Micrococcus species
Staphylococcus aureus
Corynebacterium species
Enterococcus faecalis
Lactobacillus species Paracoccus yeei Pseudomonas oryzihabitans
universally accepted guidelines for the disinfection of cell phones. The efficacy of sterilization can be defined as whether repeat cultures are positive after disinfecting the tested surface. Alternative studies have examined the use of adenosine triphosphate (ATP) bioluminescence to monitor the efficacy7-13. One study examined how effective decontamination was in the operating room using this system14. ATP is present in a wide variety of organic material, such as bacteria, food, and human secretions and excretions, and has been used in the food and beverage industries to assess the adequacy of cleaning procedures8,15. This surfaceswabbing technique involved a reaction of ATP with luciferin and luciferase enzyme, resulting in the emission of light. This light was then detected with use of a handheld luminometer, giving a result in only a few seconds10. A threshold between 250 and 500 relative light units indicated a clean surface12, whereas poorly cleaned surfaces yielded >1000 relative light units13. Willis et al. concluded that ATP bioluminescence was not directly equivalent to microbiological testing but was a useful tool for monitoring cleanliness10. This study investigated the presence of bacteria on cell phones in an orthopaedic operating room and the efficacy of recommended cleaning methods. Our hypothesis was that cell phones are a potential source for bacterial contamination and that a standardized disinfecting protocol would substantially decrease their rate of bacterial contamination and the amount of organic material present. We also hypothesized that the likelihood of a positive culture and the amount of organic material will remain decreased one week after disinfecting. Materials and Methods
A
fter approval from the institutional review board, the study was performed at the five operating room sites affiliated with our institution. The study enrolled all attending and resident orthopaedic surgeons at our university-based program for a total of fifty-three participants.
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an overlapping “S” pattern was used to cover the entire surface with horizontal strokes with a rolling motion to maximize contact with the surface. Then the same area was swabbed again using vertical “S” strokes, and finally the swab was rotated once more using diagonal “S” strokes (see Appendix) in accordance with 16 similar recommendations from the Centers for Disease Control and Prevention . These right-sided samples were placed into ATP bioluminescence re13 action tubes and were agitated for at least five seconds . The relative light units were immediately measured on the Clean-Trace Luminometers. Relative light units are measured because one photon of light is emitted for each molecule of ATP present. The left-sided samples were cultured on 5% sheep blood agar (BBL; Becton Dickinson, Sparks, Maryland) incubated at 37°C in 5% CO2 and MacConkey agar incubated at 37°C in air. Plates were examined at twenty-four and forty-eight hours, and all colony types present were subjected to Gram stain and biochemical identification. Identification was performed with use of catalase reagent (H2O2), Staphaurex (Remel, Lenexa, Kansas), and Vitek 2 (bioM´erieux, Durham, North Carolina). Susceptibility testing was performed on organisms deemed clinically meaningful with use of Vitek 2. Antimicrobials tested were based on those that would be reported for organisms in a surgical 17,18 site infection .
Cleaning Regimen and Survey The cell phones underwent a standardized disinfecting protocol with Bausch & Lomb Clens wipes (Rochester, New York). These wipes were labeled as safe for Apple products and were used for all phones because of their low concentration of alcohol to disinfect without damaging. Because all cell phones were individually owned, we chose a product that was endorsed by the manufacturer so that it would not void any warranty or damage the product. The main ingredient is 32% isopropyl alcohol and a proprietary protected detergent. The disinfecting technique was identical to the swab technique to cleanse the entire surface area of the device. After a standardized time of five minutes, which was used so that any and all residual products were not present on the sampled surface, the cell phone was tested again with use of the same technique for repeat cultures and ATP bioluminescence. During the wait time, a verbal questionnaire was given to all participants in the study on the extent of usage of their cell phones, the locations of use, the use of headsets, the awareness of disinfection practices of cell phones, and the frequency of hand-washing after 19 using their phones . One week later, all phones were then retested by swabbing for cultures and ATP bioluminescence. A second questionnaire was then given regarding whether or not their cleaning practices had changed. The bacterial growth results were further divided into pathogenic and nonpathogenic bacteria on the basis of the organisms recovered. Other common bacteria that did not grow from culture specimens from the study participants’ cell phones were omitted. These organisms were divided by those most likely to cause surgical site infection according to the Guide to the Elimination of Orthopedic Surgical Site Infections by the Association for Professionals 17,18 in Infection Control and Epidemiology (APIC) (Table I) . The ATP results were then further classified as 500 relative light units and 250 relative light units on the basis of the previously discussed ATP benchmarks, in which the threshold between 250 and 12,13 500 relative light units indicated a clean surface .
TABLE II Relative Light Units and Culture Results at Each Time Point
Sampling Protocol Each cell phone was tested, on both the front and back surfaces, in the operating room while the surgeon was scrubbed into surgery. The phone was placed on a sterile towel during testing and was handled with sterile gloves to minimize the risk of contamination. The phone was divided in half from top to bottom. The left side of the phone was swabbed for inoculation on blood and MacConkey agar and was labeled with a randomized number and a letter: A for initial, B for after disinfection, and C for one week later. The right side was swabbed for ATP bioluminescence assay (3M Clean-Trace Surface ATP; 3M, St. Paul, Minnesota). The technique was standardized and was labeled in a similar fashion. First,
Bacteria Grown on Culture Time Point Initial After disinfection One week later
Relative Light Units*
Pathogenic
Nonpathogenic
3488 ± 2998
83%
59%
200 ± 123
8%
9%
1825 ± 1699
75%
30%
*The values are given as the mean and the standard deviation.
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CELL PHON ES AS A POTEN TIA L SOU RCE OF BACTER IA L C O N TA M I N AT I O N I N T H E O P E R AT I N G R O O M
TABLE III Culture Results Based on the Type of Bacteria at Each Time Point Time Point Initial After disinfection One week later
Coagulase-Negative Staphylococci*
Viridans Streptococci*
Staphylococcus Aureus*
Enterococcus Faecalis*
40
2
4
0
6
0
1
0
39
2
4
1
*The values are given as the number of phones with positive results.
Study Population The study group consisted of fifty-three participants (forty-one male participants and twelve female participants), and there were twenty attending physicians and thirty-three residents. There were three brands of phones tested: forty-four Apple, eight Samsung, and one Blackberry (Waterloo, Ontario, Canada). There were ten different models among these manufacturers. Thirtynine of the fifty-three participants had cases on their phones, and, of those, twenty-six had “smooth” cases with no grooves or crevices and thirteen had “rough” cases with grooves or crevices. The phones were divided into three groups based on size. Size was defined as the average being the size of an iPhone 5, 5c, or 5s (Apple) (twenty-seven of fifty-three phones), which was 4.9 inches (12.5 cm) long. One group was this average size at 4.9 inches (12.5 cm), the second group was smaller than the average size at 12.5 cm).
Statistics Our primary measures were bacterial growths on culture and mean relative light units on cell phones on initial presentation. Our secondary outcome 13 measures were determination of the difference before and after cleaning . Continuous data were analyzed with use of either the paired or Student t test. The Pearson chi-square test was used for nominal data along with relative risk and its 95% confidence intervals for cutoff values of 250 and 500 relative light units and pathogenic growth. The Fisher exact test was used for analyses of categorical variables with small expected cell frequencies. Two-sided signifi-
cance was set at p < 0.05. We used a convenience sample without sample-sized calculations. Therefore, some of the analyses of predictors of contamination may be underpowered.
Source of Funding There was no source of external funding for this study.
Results he mean results (and standard deviation) were 3488 ± 2998 relative light units at the initial swab, 200 ± 123 relative light units after disinfection, and 1825 ± 1699 relative light units one week following disinfection (Table II and Fig. 1). Of the fifty-three participants who had >500 relative light units, there were fifty-two (98%) at the initial swab, one (2%) after disinfection, and forty-eight (91%) one week later. Of the fiftythree participants who had >250 relative light units, there were fifty-two (98%) at the initial swab, nine (17%) after disinfection, and fifty-one (96%) one week later. Culture specimens were taken for all fifty-three cell phones. Pathogenic bacteria grew on forty-four cultures (83%) and nonpathogenic bacteria grew on thirty-one cultures (59%) on initial swab; pathogenic bacteria grew on four cultures (8%)
T
Fig. 1
ATP mean results in relative light units (RLUs) at each time point: initial swab, after disinfection, and one week later. SD = standard deviation.
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TABLE IV Initial and One-Week Survey Questions with Results Questions
Front only
Results
2%
Front and back (snap-in with soft screen protector)
21%
4%
Complete (e.g., LifeProof)
38%
8%
Back only
40%
Texting Calling
49% 28%
Internet E-mailing
11%
What is the daily frequency of your usage? Two to five times
Questions What kind of case does your phone have?
What is the phone used for?
Once
TABLE IV (continued)
Results
Initial survey data
All
CELL PHON ES AS A POTEN TIA L SOU RCE OF BACTER IA L C O N TA M I N AT I O N I N T H E O P E R AT I N G R O O M
0%
One-week survey data Have you changed your phone-cleaning practices?
5%
Yes
13%
Six to twenty times Twenty-one to fifty times
21% 53%
No
87%
More than fifty times
21%
How often is the phone cleaned now? Never
19%
Home
9%
After every use After one to five uses
Car
0%
After six to ten uses
Gym
4%
Once a week
30%
Every couple of weeks
21%
Where is the phone most commonly used?
Hospital Where is the phone used in the hospital? Office Outside patient’s room
87% 38% 38%
Emergency room
4%
Operating room
9%
On-call room
11%
Yes No Do you know the manufacturer’s cleaning technique?
42% 58%
Yes
2%
No
98%
Do you know the hospital’s cleaning recommendations? Yes No
0% 100%
How often do you clean your hands after phone use? Never After every use
47% 0%
After two to five uses After six to ten uses
13% 4%
After every patient seen
36%
How often is the phone cleaned? Never After every use
26% 0%
After two to five uses
4%
After six to ten uses
19%
Once a week Every couple of weeks
15% 36%
continued
30%
How often do you clean your hands after phone use? Never After every use
0% 0%
After two to five uses
8%
After six to ten uses
8%
After every patient seen
Does the phone have hands-free Bluetooth?
0% 0%
84%
Have you changed your hand-washing practice? Yes No
17% 83%
and nonpathogenic bacteria grew on five cultures (9%) after disinfection; and pathogenic bacteria grew on forty cultures (75%) and nonpathogenic bacteria grew on sixteen cultures (30%) one week later. For the focus of this study, we concentrated on only pathogenic bacteria in relation to relative light units (Table III and Fig. 2). Staphylococcus aureus was identified on four cell phones both before screening and one week later but was only identified on one phone after disinfecting initially. Comparing relative light units of 500 with whether the phone grew pathogenic bacteria on culture demonstrated significance (p = 0.03) at the initial swab, but not after disinfection, and it was nearly significant (p = 0.053) one week later (see Appendix). This is consistent with expectations that, as relative light units exceed 500, there would be an increased amount of pathogenic bacterial growth as demonstrated by samples initially and one week later. Comparing relative light units of 250 with pathogenic bacterial growth on culture demonstrated significance at the initial swab but not after disinfection or after one week (see Appendix). Although forty-six (87%) of fifty-three phones had a decrease in the relative light units one week after disinfection by more than half, 75% had cultures positive for pathogenic bacteria.
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CELL PHON ES AS A POTEN TIA L SOU RCE OF BACTER IA L C O N TA M I N AT I O N I N T H E O P E R AT I N G R O O M
Fig. 2
Percentage of pathogenic and nonpathogenic bacterial results at each time point: initial swab, after disinfection, and one week later.
When looking at relative light units and bacterial growth, there was no significant difference between male and female sex (p = 0.59), between attending physicians’ cell phones and residents’ cell phones (p = 0.20), between cell phones with a case and those without a case (p = 0.11), between a smooth case and a rough case (p = 0.17), or among the three sizes of the cell phones in this study (p = 0.73) (see Appendix). Table IV demonstrates the initial and one-week survey results. On the initial survey, almost half of the physicians used their phones for texting approximately twenty-one to fifty times a day. Expectedly, most of the use was at the hospital and nearly all participants did not know what the cleaning recommendation was for their phones. Of the fifty-three participants in this study, 36% (nineteen participants) cleaned their phones every couple of weeks and 40% (twenty-one participants) had back-only cases on their phones. One week later, 87% (forty-six participants) had changed their phone-cleaning practices. Thirty percent (sixteen participants) increased their cleaning to after six to ten uses up from 19% (ten participants) before the study. Of the fifty-three participants, 30% (sixteen participants) increased their cleaning to once a week up from 15% (eight participants) before the study. Discussion e believe this to be the first study to investigate cell phones as a potential source of bacterial contamination in the operating room using both relative light units and cultures. We demonstrated that cell phones had a contamination rate of 83% (forty-four participants) based on cultures, similar to, but not as high as, previous studies2,3. On the basis of relative light units, 98% (fifty-two participants) of phones had a value greater than what is considered clean. Prior studies used various relative light unit targets ranging from 250 to 500, which have been shown to
W
indicate decreased bacterial colony counts on various inpatient care surfaces. This has been linked to incremental quality improvements13. There was a noticeable decrease in relative light units and amount of bacterial growth on culture after a simple cleanse of the phone. This small effort decreased ATP and the likelihood of pathogenic-positive cultures. A recent prevalence study found that surgical site infections were the most common health care-associated infection, accounting for 31% of all hospital-acquired infections among hospitalized patients20. The National Healthcare Safety Network data for 2006 to 2008 showed an overall surgical site infection rate of 1.9% with 16,147 surgical site infections following 849,659 operative procedures21. It is yet unknown whether there is a correlation of cell phone contamination with surgical site infection rates and/or bacteria found in surgical site infections. A weakness of our study was that we did not follow each patient to determine whether a surgical site infection developed. Therefore, no official recommendations can be made regarding cell phone use or disinfection in operating rooms. However, it seems reasonable to recommend that a surgeon disinfect his or her phone as a precautionary measure if it is going to be used in the operating room. A limitation of our study was the inability to answer the question of whether the products in the wipe itself impacted the sampling results or if the mechanical act of wiping alone would have been sufficient. Another limitation of our study was that we did not quantify bacterial growth in number of colonies. This was intended to answer the question of what is growing on cell phones of orthopaedic surgeons and not how many colonies were growing. Additional studies could quantify the number of colonies and determine if there is a correlation between the number of colonies and the number of relative light units. Additional studies could
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also evaluate the efficacy of ultraviolet light for the decontamination of cell phones. Willis et al. demonstrated inconsistent correlation between relative light unit count and positive growth on culture and concluded that ATP bioluminescence is not directly correlated to cultures; however, the instant results support its use as a beneficial tool for monitoring cleanliness10. It is also important to note that bacterial cultures do not assess for other biological contaminants such as viruses or eukaryotic cells, whereas the ATP luminometer does. One review article pooled data on mobile communication devices and, with regard to device cleaning, recommended restricting the use of cell phone technology in certain high-risk areas, such as operating rooms, intensive care units, and burn units22. In another recent study, Beckstrom et al. reviewed bacterial contamination of parents’ cell phones in a neonatal intensive care unit and the effectiveness of an anti-microbial gel in reducing transmission to the hands23. They demonstrated that all cell phones had bacterial contamination and 90% had the same bacteria on the cell phone and on the parents’ hands23. This demonstrates the need for proper hand-washing techniques as well as the importance of cell phone cleanliness because only disinfecting one or the other results in continued contamination of both. In conclusion, cell phones of orthopaedic surgeons are used commonly in the operating room and we found a high rate of pathogenic bacterial contamination and organic material on them. This bacterial and organic material load was decreased after a single disinfecting process with commercially available cleaning wipes safe for cell phone use. One week after disinfection, a cell phone had a high likelihood of bacterial recontamination, although the amount of accumulated organic material was decreased compared with that before disinfection. Although the risk that cell phones pose as a source of surgical site infections is yet unknown, to our knowledge, it seems
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prudent for surgeons who use their cell phones in the operating room to regularly disinfect them or to consider not using them at all in the operating room. Appendix A figure demonstrating the swabbing technique used on each phone for both ATP and bacterial cultures and tables showing a comparison of dichotomized pathogen counts at the three time points and demographic data are available with the online version of this article as a data supplement at jbjs.org. n NOTE: We especially thank Dr. Heidi Israel, PhD in statistics, for her help in analyzing the data. We also thank Dr. Berton R. Moed, chairman of the Department of Orthopaedic Surgery, for his expertise, guidance, and support on this project.
Irshad A. Shakir, MD Scott G. Kaar, MD Department of Orthopaedic Surgery, Saint Louis University, 3635 Vista Avenue, Desloge Towers, 7th Floor, St. Louis, MO 63110. E-mail address for S.G. Karr: [email protected] Nirav H. Patel, MD Department of Internal Medicine, Division of Infectious Diseases, Saint Louis University, 3635 Vista at Grand Boulevard, St. Louis, MO 63110 Robin R. Chamberland, PhD Department of Pathology, Saint Louis University, 1402 South Grand Boulevard, St. Louis, MO 63104
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10. Willis C, Morley R, Westbury J, Greenwood M, Pallett A. Evaluation of ATP bioluminescence swabbing as a monitoring and training tool for effective hospital cleaning. Br J Infect Control. 2007;8:17-21. 11. Sherlock O, O’Connell N, Creamer E, Humphreys H. Is it really clean? An evaluation of the efficacy of four methods for determining hospital cleanliness. J Hosp Infect. 2009 Jun;72(2):140-6. Epub 2009 Mar 24. 12. Lewis T, Griffith C, Gallo M, Weinbren M. A modified ATP benchmark for evaluating the cleaning of some hospital environmental surfaces. J Hosp Infect. 2008 Jun;69(2):156-63. Epub 2008 May 12. 13. Boyce JM, Havill NL, Dumigan DG, Golebiewski M, Balogun O, Rizvani R. Monitoring the effectiveness of hospital cleaning practices by use of an adenosine triphosphate bioluminescence assay. Infect Control Hosp Epidemiol. 2009 Jul;30 (7):678-84. 14. Vande Leest L, Kawczynski R, Esser Lipp F, Barrientos R. Identifying potential areas of infectivity on high-touch locations in the OR. AORN J. 2012 Nov;96(5):507-12. 15. Davidson CA, Griffith CJ, Peters AC, Fielding LM. Evaluation of two methods for monitoring surface cleanliness-ATP bioluminescence and traditional hygiene swabbing. Luminescence. 1999 Jan-Feb;14(1):33-8. 16. Centers for Disease Control and Prevention. Emergency response resources: Surface sampling procedures for Bacillus anthracis spores from smooth, non-porous surfaces. 2012. http://www.cdc.gov/niosh/topics/emres/surface-samplingbacillus-anthracis.html. Accessed 2014 Feb 17. 17. Greene LR. Guide to the elimination of orthopedic surgery surgical site infections: an executive summary of the Association for Professionals in Infection Control
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and Epidemiology elimination guide. Am J Infect Control. 2012 May;40(4):384-6. Epub 2011 Aug 25. 18. Greene LR, Mills R, Moss R. Association for Professionals in Infection Control and Epidemiology. Guide to the elimination of orthopedic surgical site infections. 2010. http://www.apic.org/Resource_/EliminationGuideForm/34e03612-d1e64214-a76b-e532c6fc3898/File/APIC-Ortho-Guide.pdf. Accessed 2014 Oct 3. 19. Ramesh J, Carter AO, Campbell MH, Gibbons N, Powlett C, Moseley H Sr, Lewis D, Carter T. Use of mobile phones by medical staff at Queen Elizabeth Hospital, Barbados: evidence for both benefit and harm. J Hosp Infect. 2008 Oct;70(2):160-5. Epub 2008 Aug 12. 20. Magill SS, Hellinger W, Cohen J, Kay R, Bailey C, Boland B, Carey D, de Guzman J, Dominguez K, Edwards J, Goraczewski L, Horan T, Miller M, Phelps M, Saltford R, Seibert J, Smith B, Starling P, Viergutz B, Walsh K, Rathore M, Guzman N,
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Fridkin S. Prevalence of healthcare-associated infections in acute care hospitals in Jacksonville, Florida. Infect Control Hosp Epidemiol. 2012 Mar;33(3):283-91. Epub 2012 Jan 12. 21. Mu Y, Edwards JR, Horan TC, Berrios-Torres SI, Fridkin SK. Improving riskadjusted measures of surgical site infection for the National Healthcare Safety Network. Infect Control Hosp Epidemiol. 2011 Oct;32(10):970-86. Epub 2011 Sep 1. 22. Brady RR, Verran J, Damani NN, Gibb AP. Review of mobile communication devices as potential reservoirs of nosocomial pathogens. J Hosp Infect. 2009 Apr;71(4):295-300. Epub 2009 Jan 24. 23. Beckstrom AC, Cleman PE, Cassis-Ghavami FL, Kamitsuka MD. Surveillance study of bacterial contamination of the parent’s cell phone in the NICU and the effectiveness of an anti-microbial gel in reducing transmission to the hands. J Perinatol. 2013 Dec;33(12):960-3. Epub 2013 Sep 5.
