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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 microor-
ganisms. We investigated the rate of potentially pathogenic bacteria present on uniforms worn by hospital staff, as well as the bac-
terial 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 or-
ganisms. 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 con- admit many elderly patients, including many from
tamination of the uniforms and clothing of health nursing homes.9,10 This patient population has a signif-
care workers (HCWs) during patient care activities.1-4 icant rate of colonization with resistant bacteria on ad-
Physicians’ white coats2,5 and ties,6,7 medical students’ mission to the hospital, which increases during
coats,4 and nurses’ uniforms1,3 have all been shown to hospitalization.11,12 Despite continuing efforts to im-
be colonized with pathogenic organisms and thus may prove infection control measures, HCWs may uninten-
be a potential source of cross-infection. The maximal tionally carry bacteria on their attire, including nurses’
contamination occurs in areas of greatest hand contact uniforms and physicians’ white coats. Nevertheless,
(ie, pockets and cuffs), allowing recontamination of few organizations have made recommendations for
already washed hands.1,2,4 provision and exchange of HCWs’ clothing.13
With the increasing prevalence of multidrug- We assessed the rate of contamination of uniforms
resistant bacteria in hospital settings, investigating with potentially pathogenic bacteria, comparing attire
the role of environmental factors, including staff attire, worn by nurses and physicians, and semiquantitatively
in the spread of infection is important.8 The medical determined the bacterial load on uniforms.
departments of our hospital, like those of many others,
METHODS
From the Infectious Disease Unit,a Shaare Zedek Nursing School,b and
Clinical Microbiology Laboratory,c Shaare Zedek Medical Center, Setting
Hebrew University‒Hadassah Medical School, Jerusalem, Israel.
The study was conducted in a 550-bed, university-
Address correspondence to Yonit Wiener-Well, MD, Infectious Disease
Unit, Shaare Zedek Medical Center, PO Box 3235, Jerusalem 91301, affiliated hospital, Jerusalem’s second largest. The Divi-
Israel. E-mail: yonitw@zahav.net.il. sion of Internal Medicine consists of 5 departments,
Presented as an abstract at the 48th Interscience Conference on Anti- and the surgical wing includes a general surgery de-
microbial Agents and Chemotherapy, Washington, DC, October 25-28, partment and departments for orthopedics, obstetrics,
2008. urology, otorrhinolaryngology, ophthalmology, plastic
Conflict of interest: None to report. surgery, and cardiac surgery.
0196-6553/$36.00
Copyright ª 2011 by the Association for Professionals in Infection
Enrolled staff
Control and Epidemiology, Inc. Published by Elsevier Inc. All rights
reserved.
A total of 135 physicians and nurses from the med-
ical and surgical wings were included in this study. We
doi:10.1016/j.ajic.2010.12.016
used a convenience sample, including all subjects on

555
556 Wiener-Well et al. American Journal of Infection Control
September 2011

duty at the time of sampling. Less than 5% of the staff and confirmed by the double-disc method.14,15 Gram-
refused to take part in this study. Each participant com- negative bacteria were identified using the API Kit
pleted a questionnaire with items evaluating how long (bioMerieux, Marcy l’Etiole, France).
the participant had been wearing his or her current at-
tire, how frequently he or she changes attire, and how
Definition of bacteria
he or she would rate the attire’s level of hygiene.
The recovered bacteria were classified into 2 groups:
Definition of uniforms (1) nonpathogenic skin flora, including coagulase-
negative staphylococci, Bacillus spp, Micrococcus spp,
Physicians wear long-sleeved white coats on top of diphtheroids, lactose-nonfermenting gram-negative
their own clothes; each individual determines the fre- bacilli (except for Pseudomonas and Acinetobacter)
quency of coat changes. Nurses wear 2-piece uniforms, and Streptococcus viridians, and (2) pathogenic bacte-
which they change daily. Operating room 2-piece scrub ria, including S aureus, Enterobacteriaceae, Pseudomo-
suits are used by physicians and nurses, and are changed nas, and Acinetobacter spp.
daily. All uniforms are provided by the hospital. Resistant pathogenic bacteria were defined as
methicillin-resistant S aureus (MRSA); vancomycin-
Sampling resistant Enterococcus; extended spectrum b-lactamase–
producing Enterobacteriaceae; Pseudomonas resistant to
Individual impressions were taken from different gentamicin, ciprofloxacin, and ceftazidime; and Acineto-
sites of white coat or uniforms, using 9 cm2 plates con- bacter resistant to meropenem.
taining 5% tryptic soy blood agar pressed for 10 sec-
onds, as described previously.2,4 All participants were
sampled on the mid-abdominal zone, at umbilical Statistical analysis
height. The second sampling site was either the termi- All statistical analyses were done using the x2 test for
nal portion of sleeves or, for a short-sleeved uniform, dichotomous variables and the Mann-Whitney U test
the side pockets. The dominant side of the participant for continuous variables. A P value ,.05 was consid-
was chosen for sampling of sleeve ends and pockets. ered to indicate statistical significance.
Each participant was sampled at 2 areas, except for
staff wearing operating room scrub suits, which were RESULTS
sampled only at the abdominal site, because these suits
do not have long sleeves or pockets. A total of 238 samples were obtained from 135 per-
As a control, we cultured 4 randomly chosen uni- sonnel, including 60 (45%) physicians and 75 (55%)
forms immediately on receipt from the hospital laun- nurses. Of the participants, 85 (63%) were female, 88
dry and before use. (65%) were age .30 years, and 73 (54%) had .5 years
of working experience. Sixty percent worked in surgical
Microbiological evaluation departments and 40% worked in medical departments.
Seventy-nine participants (58%) reported changing his
Plates were incubated for 48 hours at 358C and or her uniform every day, and 104 (77%) rated his or
then examined for total colony count. Organisms her uniform as moderately clean to very clean (Table 1).
were Gram-stained and identified by standard microbi- Nonpathogenic skin bacteria were isolated and iden-
ological methods. Antibiotic sensitivity was tested on tified from all gown cultures (100%), but these data are
Iso-sensitest agar by the Kirby-Bauer disc-diffusion not reported here. These contaminants included
method. Staphylococci were identified as Staphylococ- coagulase-negative staphylococci (in 50% of samples),
cus aureus using Pastorex Staph-Plus (Bio-Rad, Marnes- Bacillus spp (20%), Micrococcus (18%), diphtheroids,
la-Coquette, France), and methicillin resistance was lactose-nonfermenting gram-negative bacilli (exclud-
determined by growth on Mueller-Hinton agar contain- ing Pseudomonas and Acinetobacter), Streptococcus
ing 4% sodium chloride and 6 mg/mL of oxacillin. viridans, and others.
Vancomycin-resistant enterococci were identified by Of the 238 samples obtained, 119 (50%) were posi-
growth on enterococcal agar (BD Microbiology Sys- tive for any pathogen, most with one pathogen (94 cul-
tems, Sparks, Maryland), containing 6 mg/mL of vanco- tures; 79% of the positive cultures) and fewer with 2 or
mycin and by analysis with Etest (AB Biodisk, Solna, 3 different pathogens (21 [18%] and 4 [3%] of the pos-
Sweden). Extended-spectrum b-lactamase producing itive cultures, respectively). There were no significant
Enterobacteriaceae were isolated using MacConkey differences between physicians and nurses. Potentially
agar containing 2 mg/mL of ceftazidime and brain pathogenic bacteria were isolated from at least one site
heart infusion broth containing 2 mg/mL of ceftazidime, of the gowns in 85 of the 135 participants (63%), 49
www.ajicjournal.org Wiener-Well et al. 557
Vol. 39 No. 7

Table 1. Risk factors and distribution of different pathogens isolated from attire cultures (n 5 238)
Cultures with
Cultures with Acinetobacter, S aureus, Enterobacteriaceae, Pseudomonas, resistant
Variable (n) pathogens, n (%)* n (%) n (%) n (%) n (%) pathogens, n (%)y

Profession
Physicians (60) 44 (48) 29 (31) 17 (18) 7 (8) 3 (3) 6 (6)
Nurses (75) 75 (51) 60 (41) 15 (10) 11(8) 5 (3) 21 (14)
Sex
Female (85) 83 (51) 60 (37) 19 (12) 16 (10) 6 (4) 17 (10)
Male (50) 36 (48) 29 (39) 13 (17) 2 (3) 2 (3) 10 (13)
Wing
Surgery (81) 62 (46) 51 (38) 12 (9) 7 (5) 7 (5) 11 (8)
Internal medicine (54) 57 (55) 38 (37) 20 (19) 11 (11) 1 (1) 16 (15)
Age, years
#30 (47) 33 (39) 25 (29) 9 (11) 4 (5) 0 (0) 8 (9)
31-40 (48) 46 (53) 32 (37) 15 (17) 8 (9) 3 (3) 12 (14)
41-50 (30) 32 (64) 25 (50) 6 (12) 5 (10) 5 (10) 7 (14)
$51 (10) 8 (47) 7 (41) 2 (12) 1 (6) 0 (0) 0 (0)
Seniority, years
#5 (62) 51 (47) 38 (35) 14 (13) 8 (7) 3 (3) 12 (11)
6-10 (23) 19 (45) 14 (33) 9 (21) 2 (5) 0 (0) 5 (12)
11-20 (32) 31 (52) 23 (38) 4 (2) 6 (10) 4 (7) 7 (12)
$21 (18) 18 (67) 14 (52) 5 (19) 2 (7) 1 (4) 3 (11)
Type of attire
White coat (26) 28 (54) 17 (32) 10 (19) 4 (8) 1 (2) 3 (6)
Uniforms (77) 75 (49) 58 (38) 18 (12) 13 (8) 5 (3) 21 (14)
Operating room uniforms (32) 16 (50) 14 (43) 4 (13) 1 (3) 2 (6) 3 (9)
Frequency of attire changes, days
1 (79) 58 (46) 44 (35) 15 (12) 8 (6) 6 (5) 10 (8)x
2 (20) 27 (66) 23 (56) 5 (12) 5 (12) 1 (2) 12 (29)x
3 (12) 9 (44) 7 (32) 2 (9) 1 (5) 1 (5) 2 (9)
4-7 (19) 18 (47) 9 (24) 8 (21) 4 (11) 0 (0) 2 (5)
$8 (5) 7 (70) 6 (60) 2 (20) 0 (0) 0 (0) 1 (10)
Cleanliness of attirez
Clean (51) 40 (45) 32 (36) 13 (15) 5 (6) 2 (2) 13 (14)
Moderate (53) 51 (55) 34 (37) 12 (13) 11 (12) 5 (5) 6 (7)
Not clean (31) 28 (48) 23 (40) 7 (12) 2 (3) 1 (2) 4 (14)
Sample site
Abdomen (135) 68 (50) 55 (41) 15 (11) 10 (7) 5 (4) 11 (8)
Sleeve (21) 10 (48) 6 (29) 4 (19) 2 (10) 0 (0) 2 (10)
Pocket (82) 41 (50) 28 (34) 13 (16) 6 (7) 3 (4) 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 departments compared with operating room scrub
physicians (60% of participating physicians). suits (14% vs 9%), and on pockets compared with ab-
We assessed various demographic and clinical risk dominal zones and sleeve ends (17% vs 8% and 10%,
factors for isolation of any pathogen or resistant path- respectively). The frequency of attire changes attire
ogen from gown cultures and found no significant risk was the only risk factor that reached statistical signifi-
factors for isolation of any pathogen from gown cul- cance. No correlation was found between the rate of
tures (Table 1). The rate of contamination with resistant cultures positive for resistant pathogens and the per-
pathogens was higher in attire changed every 2 days sonnels’ age, seniority, or rating of their attire’s
compared with that changed every day (29% vs 8%; cleanliness.
P , .05), in cultures from nurses’ uniforms compared Isolated pathogenic bacteria were divided into
with physicians’ uniforms (14% vs 6%), in male per- 4 groups; their distribution is given in Table 2. Acineto-
sonnel compared with female personnel (13% vs bacter spp were the most common isolated pathogenic
10%), in medical departments compared with surgical bacteria (89/238 cultures; 37%), followed by S aureus
departments (15% vs 8%), in uniforms worn in the (32/238 cultures; 13%), Enterobacteriaceae (18/238
558 Wiener-Well et al. American Journal of Infection Control
September 2011

cultures; 8%), and Pseudomonas (8/238 cultures; 3%). Table 2. Bacterial load of different pathogens isolated
The highest mean bacterial load (number of colony- from gown cultures (n 5 147)
forming units [CFU] per culture plate) was found for
Colonies/plate,
S aureus (14 6 18 CFU), with a higher load for MRSA Bacteria (number of isolates) mean 6 SD (range)
than for methicillin-sensitive S aureus (21 6 28 CFU
vs 11 6 13 CFU) (Table 2). Acinetobacter (89) 4 6 6 (1-36)
Only common skin bacteria were isolated from the A baumannii (31) 4 6 8 (1-36)
A lwoffi (58) 4 6 4 (1-18)
control sample of 4 uniforms cultured immediately af- Staphylococcus aureus (32) 14 6 18 (1-80)
ter receipt from the hospital laundry but before use. Methicillin-sensitive S aureus (24) 11 6 13 (1-62)
Bacterial loads were significantly lower than on the MRSA (8) 21 6 28 (2-80)
uniforms being worn. Enterobacteriaceae (18) 5 6 8 (1-33)
Enterobacter cloacae (7) 4 6 5 (1-14)
Klebsiella pneumoniae (6) 9 6 12 (1-33)
DISCUSSION Klebsiella oxytoca (2) 1 (1-1)
Citrobacter freundii (1) 2
The role of HCWs’ attire in the transmission of bacteria Escherichia coli (1) 2
and development of nosocomial infections is not clear. Pantoea agglomerans (1) 1
Several studies found frequent contamination of nurses’ Pseudomonas (8) 3 6 2 (1-6)
P stutzeri (4) 2 6 2 (1-4)
uniforms16 and transmission of bacteria through the P putida (2) 5 6 1 (4-6)
textile of uniforms,17 with varying efficiencies of fabrics P aeruginosa (1) 3
used as barriers for bacterial transfer.18,19 One study con- P fluorescens (1) 2
ducted 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 to be determined. S aureus, especially MRSA, was asso-
cross-contamination between burn patients compared ciated with higher bacterial load compared with other
with a plastic isolation tent.21 pathogenic bacteria evaluated in the present study as
Other studies have reported conflicting findings re- well as compared with results of a previous study.2
garding the role of HCWs’ attire in transmission of bac- Quite likely, the more significant the pathogenic bacte-
teria. Tammelin et al22 investigated the possibility of rial load, the more efficient the transmission from
reducing wound contamination during cardiothoracic HCWs’ uniforms to patients. We did not culture for na-
surgery through the use of special scrub suits. The sal or throat carriage of S aureus, but previous stud-
use of tightly woven scrub suits did not reduce the air ies2,16 found that only 20%-35% of S aureus isolates
count or wound contamination with methicillin- from coats had the same phage type as those cultured
resistant Staphylococcus epidermidis. Patients’ chest from the subjects’ noses. These data suggest that per-
skin was the main source of wound contamination. sonnel attire may be one route by which pathogenic
We found that HCWs’ coats and uniforms were fre- bacteria are transmitted to patients. In contrast to a pre-
quently contaminated with potentially pathogenic bac- vious study,4 the staff’s perception of their attire’s
teria; 85 of 135 uniforms (63%) and 50% of all samples cleanliness did not correlate with isolation of patho-
(238) were positive for pathogenic organisms, 11% of genic bacteria.
which were multidrug-resistant. Our data show a This study has several limitations. First, the fre-
higher incidence of contaminated uniforms than re- quency with which HCWs changed their uniforms
ported previously;1,2,4 however, some of the previous was only estimated, and we could not determine the
studies cultured only for S aureus on coats or included exact number of days that each item had been used be-
medical students and not nurses or physicians. An- fore sampling. Second, our control sample comprised
other study reported a similar high incidence (54%) only 4 clean uniforms obtained directly from the hos-
of pathogenic and even resistant bacteria, including pital laundry. We did not examine all uniforms after
vancomycin-resistant enterococci, MRSA, and Clostrid- laundering and before work, and thus the efficiency
ium difficile.3 of the laundry was only partially assessed. Third, our
The high prevalence of contaminated uniforms hospital supplies laundry service to approximately
might be related to inadequate compliance with hand 60% of its staff, whereas the remainder choose to use
hygiene, given that the sampled sites (ie, abdominal domestic laundry. Our participants were not asked
zone, sleeve ends, and pockets on the dominant side) whether they used the hospital service or washed their
are characterized by frequent hand touches. Whether uniforms at home. Concern has been expressed that
high compliance with hand hygiene practices is associ- domestic washing machines do not provide sufficient
ated with reduced bacterial load on uniforms remains decontamination of staff clothing; however, a recently
www.ajicjournal.org Wiener-Well et al. 559
Vol. 39 No. 7

published review suggests that they may be ade- 8. Zachary KC, Bayne PS, Morrison VJ, Ford DS, Silver LC, Hooper DC.
quate.23 Finally, there could have been a selection Contamination of gowns, gloves, and stethoscopes with vancomycin-
resistant enterococci. Infect Control Hosp Epidemiol 2001;22:560-4.
bias, due to the fact that personnel were chosen by con- 9. Raveh D, Gratch L, Yinnon AM, Sonnenblick M. Demographic and clin-
venience, although ,5% refused to participate. A ical characteristics of patients admitted to medical departments. J Eval
larger study, including all physicians and nurses from Clin Pract 2005;11:33-44.
all departments, could have been more representative. 10. Sonnenblick M, Raveh D, Gratch L, Yinnon AM. Clinical and demo-
In summary, we isolated potentially pathogenic bac- graphic characteristics of elderly patients hospitalized in an internal
medicine department in Israel. Int J Clin Pract 2007;61:247-54.
teria from 63% of sampled uniforms, with no signifi- 11. Benenson S, Yinnon AM, Schlesinger Y, Rudensky B, Raveh D. Optimi-
cant differences between nurses and physicians or zation of empirical antibiotic selection for suspected Gram-negative
between staff from medical departments and surgical bacteremia in the emergency department. Int J Antimicrob Agent
departments. Antibiotic-resistant bacteria were isolated 2005;25:398-403.
from samples from 14% of nurses’ uniforms and 6% of 12. Friedmann R, Raveh D, Zartzer E, Rudensky B, Broide E, Attias D,
et al. Prospective evaluation of colonization with extended-spectrum
physicians’ uniforms. Whether HCWs’ clothes play a b-lactamase (ESBL)-producing Enterobacteriaceae among patients at
major role in the transmission of pathogens to patients hospital admission and of subsequent colonization with ESBL-
and development of nosocomial infections is not clear. producing Enterobacteriaceae among patients during hospitalization.
Nonetheless, we believe that data suffice to formulate Infect Control Hosp Epidemiol 2009;30:534-42.
recommendations regarding HCWs’ uniforms. Wearing 13. British Medical Association. Uniform and dress code for doctors: guid-
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