Nursing and physician attire as possible source of nosocomial infections Yonit Wiener-Well, MD,a Margalit Galuty, RN, MSc,a,b Bernard Rudensky, PhD,c Yechiel Schlesinger, MD,a Denise Attias, BSc,c and Amos M. Yinnon, MDa Jerusalem, Israel

Background: Uniforms worn by medical and nursing staff are not usually considered important in the transmission of microorganisms. We investigated the rate of potentially pathogenic bacteria present on uniforms worn by hospital staff, as well as the bacterial load of these microorganisms. Methods: Cultures were obtained from uniforms of nurses and physicians by pressing standard blood agar plates at the abdominal zone, sleeve ends, and pockets. Each participant completed a questionnaire. Results: A total of 238 samples were collected from 135 personnel, including 75 nurses (55%) and 60 physicians (45%). Of these, 79 (58%) claimed to change their uniform every day, and 104 (77%) defined the level of hygiene of their attire as fair to excellent. Potentially pathogenic bacteria were isolated from at least one site of the uniforms of 85 participants (63%) and were isolated from 119 samples (50%); 21 (14%) of the samples from nurses’ gowns and 6 (6%) of the samples from physicians’ gowns (P 5 NS) included of antibiotic-resistant bacteria. Conclusion: Up to 60% of hospital staff’s uniforms are colonized with potentially pathogenic bacteria, including drug-resistant organisms. It remains to be determined whether these bacteria can be transferred to patients and cause clinically relevant infection. Key Words: Uniform; attire; pathogenic bacteria; nosocomial infection. Copyright ª 2011 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. (Am J Infect Control 2011;39:555-9.)

Several studies have demonstrated bacterial contamination of the uniforms and clothing of health care workers (HCWs) during patient care activities.1-4 Physicians’ white coats2,5 and ties,6,7 medical students’ coats,4 and nurses’ uniforms1,3 have all been shown to be colonized with pathogenic organisms and thus may be a potential source of cross-infection. The maximal contamination occurs in areas of greatest hand contact (ie, pockets and cuffs), allowing recontamination of already washed hands.1,2,4 With the increasing prevalence of multidrugresistant bacteria in hospital settings, investigating the role of environmental factors, including staff attire, in the spread of infection is important.8 The medical departments of our hospital, like those of many others, From the Infectious Disease Unit,a Shaare Zedek Nursing School,b and Clinical Microbiology Laboratory,c Shaare Zedek Medical Center, Hebrew University‒Hadassah Medical School, Jerusalem, Israel. Address correspondence to Yonit Wiener-Well, MD, Infectious Disease Unit, Shaare Zedek Medical Center, PO Box 3235, Jerusalem 91301, Israel. E-mail: [email protected]. Presented as an abstract at the 48th Interscience Conference on Antimicrobial Agents and Chemotherapy, Washington, DC, October 25-28, 2008. Conflict of interest: None to report. 0196-6553/$36.00 Copyright ª 2011 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. doi:10.1016/j.ajic.2010.12.016

admit many elderly patients, including many from nursing homes.9,10 This patient population has a significant rate of colonization with resistant bacteria on admission to the hospital, which increases during hospitalization.11,12 Despite continuing efforts to improve infection control measures, HCWs may unintentionally carry bacteria on their attire, including nurses’ uniforms and physicians’ white coats. Nevertheless, few organizations have made recommendations for provision and exchange of HCWs’ clothing.13 We assessed the rate of contamination of uniforms with potentially pathogenic bacteria, comparing attire worn by nurses and physicians, and semiquantitatively determined the bacterial load on uniforms.

METHODS Setting The study was conducted in a 550-bed, universityaffiliated hospital, Jerusalem’s second largest. The Division of Internal Medicine consists of 5 departments, and the surgical wing includes a general surgery department and departments for orthopedics, obstetrics, urology, otorrhinolaryngology, ophthalmology, plastic surgery, and cardiac surgery.

Enrolled staff A total of 135 physicians and nurses from the medical and surgical wings were included in this study. We used a convenience sample, including all subjects on 555

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duty at the time of sampling. Less than 5% of the staff refused to take part in this study. Each participant completed a questionnaire with items evaluating how long the participant had been wearing his or her current attire, how frequently he or she changes attire, and how he or she would rate the attire’s level of hygiene.

Definition of uniforms Physicians wear long-sleeved white coats on top of their own clothes; each individual determines the frequency of coat changes. Nurses wear 2-piece uniforms, which they change daily. Operating room 2-piece scrub suits are used by physicians and nurses, and are changed daily. All uniforms are provided by the hospital.

Sampling Individual impressions were taken from different sites of white coat or uniforms, using 9 cm2 plates containing 5% tryptic soy blood agar pressed for 10 seconds, as described previously.2,4 All participants were sampled on the mid-abdominal zone, at umbilical height. The second sampling site was either the terminal portion of sleeves or, for a short-sleeved uniform, the side pockets. The dominant side of the participant was chosen for sampling of sleeve ends and pockets. Each participant was sampled at 2 areas, except for staff wearing operating room scrub suits, which were sampled only at the abdominal site, because these suits do not have long sleeves or pockets. As a control, we cultured 4 randomly chosen uniforms immediately on receipt from the hospital laundry and before use.

Microbiological evaluation Plates were incubated for 48 hours at 358C and then examined for total colony count. Organisms were Gram-stained and identified by standard microbiological methods. Antibiotic sensitivity was tested on Iso-sensitest agar by the Kirby-Bauer disc-diffusion method. Staphylococci were identified as Staphylococcus aureus using Pastorex Staph-Plus (Bio-Rad, Marnesla-Coquette, France), and methicillin resistance was determined by growth on Mueller-Hinton agar containing 4% sodium chloride and 6 mg/mL of oxacillin. Vancomycin-resistant enterococci were identified by growth on enterococcal agar (BD Microbiology Systems, Sparks, Maryland), containing 6 mg/mL of vancomycin and by analysis with Etest (AB Biodisk, Solna, Sweden). Extended-spectrum b-lactamase producing Enterobacteriaceae were isolated using MacConkey agar containing 2 mg/mL of ceftazidime and brain heart infusion broth containing 2 mg/mL of ceftazidime,

and confirmed by the double-disc method.14,15 Gramnegative bacteria were identified using the API Kit (bioMerieux, Marcy l’Etiole, France).

Definition of bacteria The recovered bacteria were classified into 2 groups: (1) nonpathogenic skin flora, including coagulasenegative staphylococci, Bacillus spp, Micrococcus spp, diphtheroids, lactose-nonfermenting gram-negative bacilli (except for Pseudomonas and Acinetobacter) and Streptococcus viridians, and (2) pathogenic bacteria, including S aureus, Enterobacteriaceae, Pseudomonas, and Acinetobacter spp. Resistant pathogenic bacteria were defined as methicillin-resistant S aureus (MRSA); vancomycinresistant Enterococcus; extended spectrum b-lactamase– producing Enterobacteriaceae; Pseudomonas resistant to gentamicin, ciprofloxacin, and ceftazidime; and Acinetobacter resistant to meropenem.

Statistical analysis All statistical analyses were done using the x2 test for dichotomous variables and the Mann-Whitney U test for continuous variables. A P value ,.05 was considered to indicate statistical significance.

RESULTS A total of 238 samples were obtained from 135 personnel, including 60 (45%) physicians and 75 (55%) nurses. Of the participants, 85 (63%) were female, 88 (65%) were age .30 years, and 73 (54%) had .5 years of working experience. Sixty percent worked in surgical departments and 40% worked in medical departments. Seventy-nine participants (58%) reported changing his or her uniform every day, and 104 (77%) rated his or her uniform as moderately clean to very clean (Table 1). Nonpathogenic skin bacteria were isolated and identified from all gown cultures (100%), but these data are not reported here. These contaminants included coagulase-negative staphylococci (in 50% of samples), Bacillus spp (20%), Micrococcus (18%), diphtheroids, lactose-nonfermenting gram-negative bacilli (excluding Pseudomonas and Acinetobacter), Streptococcus viridans, and others. Of the 238 samples obtained, 119 (50%) were positive for any pathogen, most with one pathogen (94 cultures; 79% of the positive cultures) and fewer with 2 or 3 different pathogens (21 [18%] and 4 [3%] of the positive cultures, respectively). There were no significant differences between physicians and nurses. Potentially pathogenic bacteria were isolated from at least one site of the gowns in 85 of the 135 participants (63%), 49

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Table 1. Risk factors and distribution of different pathogens isolated from attire cultures (n 5 238)

Variable (n) Profession Physicians (60) Nurses (75) Sex Female (85) Male (50) Wing Surgery (81) Internal medicine (54) Age, years #30 (47) 31-40 (48) 41-50 (30) $51 (10) Seniority, years #5 (62) 6-10 (23) 11-20 (32) $21 (18) Type of attire White coat (26) Uniforms (77) Operating room uniforms (32) Frequency of attire changes, days 1 (79) 2 (20) 3 (12) 4-7 (19) $8 (5) Cleanliness of attirez Clean (51) Moderate (53) Not clean (31) Sample site Abdomen (135) Sleeve (21) Pocket (82)

Cultures with pathogens, n (%)*

Acinetobacter, n (%)

S aureus, n (%)

Enterobacteriaceae, n (%)

Pseudomonas, n (%)

Cultures with resistant pathogens, n (%)y

44 (48) 75 (51)

29 (31) 60 (41)

17 (18) 15 (10)

7 (8) 11(8)

3 (3) 5 (3)

6 (6) 21 (14)

83 (51) 36 (48)

60 (37) 29 (39)

19 (12) 13 (17)

16 (10) 2 (3)

6 (4) 2 (3)

17 (10) 10 (13)

62 (46) 57 (55)

51 (38) 38 (37)

12 (9) 20 (19)

7 (5) 11 (11)

7 (5) 1 (1)

11 (8) 16 (15)

33 (39) 46 (53) 32 (64) 8 (47)

25 32 25 7

(29) (37) (50) (41)

9 (11) 15 (17) 6 (12) 2 (12)

4 (5) 8 (9) 5 (10) 1 (6)

0 3 5 0

(0) (3) (10) (0)

8 12 7 0

(9) (14) (14) (0)

51 (47) 19 (45) 31 (52) 18 (67)

38 14 23 14

(35) (33) (38) (52)

14 (13) 9 (21) 4 (2) 5 (19)

8 (7) 2 (5) 6 (10) 2 (7)

3 0 4 1

(3) (0) (7) (4)

12 5 7 3

(11) (12) (12) (11)

28 (54) 75 (49) 16 (50)

17 (32) 58 (38) 14 (43)

10 (19) 18 (12) 4 (13)

58 (46) 27 (66) 9 (44) 18 (47) 7 (70)

44 (35) 23 (56) 7 (32) 9 (24) 6 (60)

15 (12) 5 (12) 2 (9) 8 (21) 2 (20)

40 (45) 51 (55) 28 (48)

32 (36) 34 (37) 23 (40)

68 (50) 10 (48) 41 (50)

55 (41) 6 (29) 28 (34)

4 (8) 13 (8) 1 (3)

1 (2) 5 (3) 2 (6)

3 (6) 21 (14) 3 (9)

8 (6) 5 (12) 1 (5) 4 (11) 0 (0)

6 (5) 1 (2) 1 (5) 0 (0) 0 (0)

10 (8)x 12 (29)x 2 (9) 2 (5) 1 (10)

13 (15) 12 (13) 7 (12)

5 (6) 11 (12) 2 (3)

2 (2) 5 (5) 1 (2)

13 (14) 6 (7) 4 (14)

15 (11) 4 (19) 13 (16)

10 (7) 2 (10) 6 (7)

5 (4) 0 (0) 3 (4)

11 (8) 2 (10) 14 (17)

*Number of cultures with pathogens is lower than the sum of 4 pathogens due to more than one pathogen in some of the cultures. y Definition of resistant pathogen: see Materials and Methods. z As defined by the owner of the attire. x P , .05 for the difference between changing attire daily and every other day.

from nurses (65% of participating nurses) and 36 from physicians (60% of participating physicians). We assessed various demographic and clinical risk factors for isolation of any pathogen or resistant pathogen from gown cultures and found no significant risk factors for isolation of any pathogen from gown cultures (Table 1). The rate of contamination with resistant pathogens was higher in attire changed every 2 days compared with that changed every day (29% vs 8%; P , .05), in cultures from nurses’ uniforms compared with physicians’ uniforms (14% vs 6%), in male personnel compared with female personnel (13% vs 10%), in medical departments compared with surgical departments (15% vs 8%), in uniforms worn in the

departments compared with operating room scrub suits (14% vs 9%), and on pockets compared with abdominal zones and sleeve ends (17% vs 8% and 10%, respectively). The frequency of attire changes attire was the only risk factor that reached statistical significance. No correlation was found between the rate of cultures positive for resistant pathogens and the personnels’ age, seniority, or rating of their attire’s cleanliness. Isolated pathogenic bacteria were divided into 4 groups; their distribution is given in Table 2. Acinetobacter spp were the most common isolated pathogenic bacteria (89/238 cultures; 37%), followed by S aureus (32/238 cultures; 13%), Enterobacteriaceae (18/238

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cultures; 8%), and Pseudomonas (8/238 cultures; 3%). The highest mean bacterial load (number of colonyforming units [CFU] per culture plate) was found for S aureus (14 6 18 CFU), with a higher load for MRSA than for methicillin-sensitive S aureus (21 6 28 CFU vs 11 6 13 CFU) (Table 2). Only common skin bacteria were isolated from the control sample of 4 uniforms cultured immediately after receipt from the hospital laundry but before use. Bacterial loads were significantly lower than on the uniforms being worn.

DISCUSSION The role of HCWs’ attire in the transmission of bacteria and development of nosocomial infections is not clear. Several studies found frequent contamination of nurses’ uniforms16 and transmission of bacteria through the textile of uniforms,17 with varying efficiencies of fabrics used as barriers for bacterial transfer.18,19 One study conducted in a burn unit demonstrated the possibility of transferring S aureus from nurses’ gowns to patients and bed sheets,20 and covering up with plastic aprons was found to more effectively prevent cloth-borne cross-contamination between burn patients compared with a plastic isolation tent.21 Other studies have reported conflicting findings regarding the role of HCWs’ attire in transmission of bacteria. Tammelin et al22 investigated the possibility of reducing wound contamination during cardiothoracic surgery through the use of special scrub suits. The use of tightly woven scrub suits did not reduce the air count or wound contamination with methicillinresistant Staphylococcus epidermidis. Patients’ chest skin was the main source of wound contamination. We found that HCWs’ coats and uniforms were frequently contaminated with potentially pathogenic bacteria; 85 of 135 uniforms (63%) and 50% of all samples (238) were positive for pathogenic organisms, 11% of which were multidrug-resistant. Our data show a higher incidence of contaminated uniforms than reported previously;1,2,4 however, some of the previous studies cultured only for S aureus on coats or included medical students and not nurses or physicians. Another study reported a similar high incidence (54%) of pathogenic and even resistant bacteria, including vancomycin-resistant enterococci, MRSA, and Clostridium difficile.3 The high prevalence of contaminated uniforms might be related to inadequate compliance with hand hygiene, given that the sampled sites (ie, abdominal zone, sleeve ends, and pockets on the dominant side) are characterized by frequent hand touches. Whether high compliance with hand hygiene practices is associated with reduced bacterial load on uniforms remains

Table 2. Bacterial load of different pathogens isolated from gown cultures (n 5 147) Bacteria (number of isolates) Acinetobacter (89) A baumannii (31) A lwoffi (58) Staphylococcus aureus (32) Methicillin-sensitive S aureus (24) MRSA (8) Enterobacteriaceae (18) Enterobacter cloacae (7) Klebsiella pneumoniae (6) Klebsiella oxytoca (2) Citrobacter freundii (1) Escherichia coli (1) Pantoea agglomerans (1) Pseudomonas (8) P stutzeri (4) P putida (2) P aeruginosa (1) P fluorescens (1)

Colonies/plate, mean 6 SD (range) 6 6 (1-36) 6 8 (1-36) 6 4 (1-18) 6 18 (1-80) 6 13 (1-62) 6 28 (2-80) 6 8 (1-33) 6 5 (1-14) 6 12 (1-33) 1 (1-1) 2 2 1 3 6 2 (1-6) 2 6 2 (1-4) 5 6 1 (4-6) 3 2

4 4 4 14 11 21 5 4 9

to be determined. S aureus, especially MRSA, was associated with higher bacterial load compared with other pathogenic bacteria evaluated in the present study as well as compared with results of a previous study.2 Quite likely, the more significant the pathogenic bacterial load, the more efficient the transmission from HCWs’ uniforms to patients. We did not culture for nasal or throat carriage of S aureus, but previous studies2,16 found that only 20%-35% of S aureus isolates from coats had the same phage type as those cultured from the subjects’ noses. These data suggest that personnel attire may be one route by which pathogenic bacteria are transmitted to patients. In contrast to a previous study,4 the staff’s perception of their attire’s cleanliness did not correlate with isolation of pathogenic bacteria. This study has several limitations. First, the frequency with which HCWs changed their uniforms was only estimated, and we could not determine the exact number of days that each item had been used before sampling. Second, our control sample comprised only 4 clean uniforms obtained directly from the hospital laundry. We did not examine all uniforms after laundering and before work, and thus the efficiency of the laundry was only partially assessed. Third, our hospital supplies laundry service to approximately 60% of its staff, whereas the remainder choose to use domestic laundry. Our participants were not asked whether they used the hospital service or washed their uniforms at home. Concern has been expressed that domestic washing machines do not provide sufficient decontamination of staff clothing; however, a recently

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published review suggests that they may be adequate.23 Finally, there could have been a selection bias, due to the fact that personnel were chosen by convenience, although ,5% refused to participate. A larger study, including all physicians and nurses from all departments, could have been more representative. In summary, we isolated potentially pathogenic bacteria from 63% of sampled uniforms, with no significant differences between nurses and physicians or between staff from medical departments and surgical departments. Antibiotic-resistant bacteria were isolated from samples from 14% of nurses’ uniforms and 6% of physicians’ uniforms. Whether HCWs’ clothes play a major role in the transmission of pathogens to patients and development of nosocomial infections is not clear. Nonetheless, we believe that data suffice to formulate recommendations regarding HCWs’ uniforms. Wearing a clean uniform daily, providing adequate laundering, improving hand hygiene practices, and using plastic aprons when performing tasks that may involve splashing or contact with body fluids likely will decrease the bacterial load on uniforms. Wearing shortsleeved coats or even having physicians discard their white coats could further reduce the cloth-borne transmission of pathogens.

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8. Zachary KC, Bayne PS, Morrison VJ, Ford DS, Silver LC, Hooper DC. Contamination of gowns, gloves, and stethoscopes with vancomycinresistant enterococci. Infect Control Hosp Epidemiol 2001;22:560-4. 9. Raveh D, Gratch L, Yinnon AM, Sonnenblick M. Demographic and clinical characteristics of patients admitted to medical departments. J Eval Clin Pract 2005;11:33-44. 10. Sonnenblick M, Raveh D, Gratch L, Yinnon AM. Clinical and demographic characteristics of elderly patients hospitalized in an internal medicine department in Israel. Int J Clin Pract 2007;61:247-54. 11. Benenson S, Yinnon AM, Schlesinger Y, Rudensky B, Raveh D. Optimization of empirical antibiotic selection for suspected Gram-negative bacteremia in the emergency department. Int J Antimicrob Agent 2005;25:398-403. 12. Friedmann R, Raveh D, Zartzer E, Rudensky B, Broide E, Attias D, et al. Prospective evaluation of colonization with extended-spectrum b-lactamase (ESBL)-producing Enterobacteriaceae among patients at hospital admission and of subsequent colonization with ESBLproducing Enterobacteriaceae among patients during hospitalization. Infect Control Hosp Epidemiol 2009;30:534-42. 13. British Medical Association. Uniform and dress code for doctors: guidance from the central consultants and specialists committee. London: British Medical Association; 2008. 14. Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing: 16th informational supplement. Wayne (PA): Clinical and Laboratory Standards Institute; 2006. p. 37. 15. Carter MW, Oakton KJ, Warner M, Livermore DM. Detection of extended-spectrum b-lactamases in Klebsiellae with the Oxoid combination disc method. J Clin Microbiol 2000;38:4228-32. 16. Speers R Jr, Shooter RA, Gaya H, Patel N, Hewitt JH. Contamination of nurses’ uniforms with Staphylococcus aureus. Lancet 1969;2:233-5. 17. Hambraeus A, Ransjo U. An instrument for measuring bacterial penetration through fabrics used for barrier clothing. J Hyg 1979;82:361-86. 18. Hambraeus A, Ransjo U. Attempts to control clothes-borne infections in burn units, I: experimental investigations of some clothes for barrier nursing. J Hyg 1977;79:193-202. 19. Lankester BJA, Bartlett GE, Garneti N, Blom AW, Bowker KE, Bannister GC. Direct measurement of bacterial penetration through surgical gowns: a new method. J Hosp Infect 2002;50:281-5. 20. Hambraeus A. Transfer of Staphylococcus aureus via nurses’ uniforms. J Hyg 1973;71:799-814. 21. Ransjo U. Attempts to control clothes-borne infections in burn units, III: an open-roofed plastic isolator or plastic aprons to prevent contact transfer of bacteria. J Hyg 1979;82:385-95. 22. Tammelin A, Hambraus A, Stahle E. Source and route of methicillinresistant Staphylococcus epidermidis transmitted to the surgical wound during cardio-thoracic surgery: possibility of preventing wound contamination by use of special scrub suits. J Hosp Infect 2001;47:266-76. 23. Wilsom JA, Loveday HP, Hoffman PN, Pratt RJ. Uniform: an evidence review of the microbiological significance of uniforms and uniform policy in the prevention and control of healthcare-associated infections. Report to the Department of Health (England). J Hosp Infect 2007; 66:301-7.