methicillin-resistant staphylococcal contamination of clothing worn by personnel in a veterinary...

Methicillin‐Resistant Staphylococcal Contamination ofClothing Worn by Personnel in a Veterinary TeachingHospitalAmeet Singh1, DVM, DVSc, Diplomate ACVS, Meagan Walker1, Joyce Rousseau2, BSc,Gabrielle J. Monteith1, BSc, and Jeffrey Scott Weese2, DVM, DVSc, Diplomate ACVIM1 Department of Clinical Studies, University of Guelph, Guelph, Canada and 2 Department of Pathobiology, Ontario Veterinary College,University of Guelph, Guelph, Canada

Corresponding AuthorAmeet Singh DVM, DVSc, Diplomate ACVS,Department of Clinical Studies, OntarioVeterinary College, University of Guelph,Guelph, Canada N1G 2W1.E‐mail: [email protected]

Submitted June 2012Accepted March 2013

DOI:10.1111/j.1532-950X.2013.12024.x

Objective: To determine the methicillin‐resistant Staphylococcus aureus (MRSA) andmethicillin‐resistant Staphylococcus pseudintermedius (MRSP) contamination rate ofwhite coats (WC) and surgical scrubs (SS) worn by personnel at the Ontario VeterinaryCollege Health Sciences Centre (OVCHSC) and to identify risk factors associated withclothing contamination.Study Design: Cross‐sectional study.Sample Population: Personnel including clinical faculty, house officers, technicians,and veterinary students working at the OVCHSC.Methods: Electrostatic cloths were used to sample WC and SS of hospital personnel.Samples were tested for MRSA and MRSP and isolates were typed. Participantscompleted a self‐administered questionnaire and data was evaluated for risk factors.Results: Of 114 specimens, MRS were isolated from 20 (17.5%), MRSA from 4(3.5%), and MRSP from 16 (14.0%). Technicians were 9.5� (OR ¼ 0.95, 95% CI:1.2–1, P ¼ .03) more likely than students to have clothing contaminated with MRSA.No risk factors were identified for MRSP or for overall MRS contamination.Conclusions: Standard hospital clothing was found to have a high prevalence of MRScontamination in a veterinary teaching hospital and could be a source of hospital‐acquired infections.

Methicillin‐resistant Staphylococcus aureus (MRSA) and meth-icillin‐resistant Staphylococcus pseudintermedius (MRSP) haveemerged as leading causes of opportunistic infections incompanion animals.1–5 Infections with these multi‐drug resistantbacteria are challenging to treat and have the potential to result inzoonotic transmission to veterinary personnel and pet owners.5–9

Considerable efforts have beenmade to increase awareness of theimplications of methicillin‐resistant staphylococcal (MRS)infections in veterinary medicine.1–3,10,11 However, thesepathogens remain a tremendous challenge to veterinarians, andmeasures to reduce and prevent MRSA and MRSP infectionsshould be emphasized in hospital infection control strategies.10,11

An important aspect of MRSA and MRSP control isidentification of potential sources of exposure. The hands ofmedical caregivers have been implicated as critical sources ofhospital‐acquired infections as they are often contaminated withopportunistic pathogens and have frequent, close contact withpatients and the hospital environment.11,12 Clothing worn byhospital personnel can also become contaminated with opportu-nistic pathogens and be a source of direct patient exposure orresult in re‐contamination of hands following appropriate handhygiene.13–19 Multi‐drug resistant bacterial contamination hasbeen reported in 4–20% of white coats and scrubs in human

hospitals.13,14,17,18 In an attempt to reduce bacterial transmissionfrom clothing to hands, the United Kingdom’s Department ofHealth has recommended a “bare below the elbows” policy inwhich white coats, long sleeve shirts, ties, jewelry, and wristwatches are not worn by hospital personnel.20 The prevalence ofbacterial contamination of hospital clothing of personnelworkingin veterinary hospitals is unknown. Considering the differencesin patient contact between human and veterinary medicine,veterinary specific data are required.

Our purpose was to determine the MRSA and MRSPcontamination rate of white coats (WC) and surgical scrubs(SS) worn by personnel at the Ontario Veterinary CollegeHealth Sciences Centre (OVCHSC) and to identify risk factorsassociated with clothing contamination.

MATERIALS AND METHODS

Sample Collection and Study Population

This cross‐sectional studywas conducted fromNovember 2011to January 2012 at the OVCHSC Small Animal Clinic.Hospital personnel, including veterinary students, technicians,

Veterinary Surgery 42 (2013) 643–648 © Copyright 2013 by The American College of Veterinary Surgeons 643

house officers (interns, residents, clinical graduate students)and senior clinicians were recruited for participation in thisstudy. Upon verbal consent, participants’ WC and/or SS weresampled using a standardized technique and a self‐adminis-tered questionnaire was completed. The questionnaire charac-terized the participants’ position in the hospital, whetherclothing had been worn from, or laundered at, home; theperception of cleanliness of the sampled clothing; and whetherthe clothing was in direct contact with an animal. Hospitalclothing at the OVCHSC included long white coats (LWC)worn by technicians, house officers, and senior clinicians; shortwhite coats (SWC) worn by veterinary students; and surgicalscrubs (SS) worn underneath laboratory coats or on their ownby all personnel depending on responsibility. Hospital clothingis provided by the OVCHSC. Laundry service is provided andinfection control protocols require that clothing not leave thebuilding; however, compliance with this protocol is variable.This study was approved by the University of Guelph ResearchEthics Board.

Microbiological Analysis

For sample collection, the participant donned nonsterileexamination gloves and wiped an electrostatic cloth (Swiffer®,Procter &Gamble, Cincinnati, OH)21–23 along the lapels, cuffs,and chest pockets of their own LC and/or the umbilical regionof SS after a short demonstration.13 After sampling, the clothwas placed into a prelabeled sterile bag. Sample collection wasobserved and coordinated by the same individual (MW).During each sampling period, new, unused, electrostatic clothswere removed from the box using a single gloved hand, placedin a sterile bag and processed in parallel with clothing samplesto act as negative control.

Enrichment culture was performed by adding 70–80 mLenrichment broth consisting of 10 g tryptone/L, 75 g sodiumchloride/L, 10 g mannitol/L, and 2.5 g yeast extract/L to thesterile bags containing electrostatic cloths immediatelyfollowing sample collection. After 24 hours incubation at35°C, 1 loopful (�10 ml) of broth was inoculated onto MRSAChromogenic agar (BBL CHROMagar MRSA, Becton,Dickinson and Company) and Mannitol Salt Agar with2 mg/mL oxacillin and incubated at 35°C. Plates wereexamined after 24 hours and 48 hours of incubation.

Isolates were identified as S. aureus by colonymorphology,Gram stain appearance, catalase reaction, coagulase reaction,and S. aureus latex agglutination test (Pastorex Staph‐plus, Bio‐Rad, Mississauga, Canada). Methicillin‐resistance was con-firmed by penicillin binding protein 2a latex agglutination test(MRSA latex agglutination test, Denka Seiken, USA, Inc.,Campbell, CA). Staphylococcus pseudintermedius was identi-fied by colony morphology, Gram stain appearance, catalase,and coagulase reactions and a species‐specific PCR assay.24

MRSA Characterization

Isolates were typed by sequencing of theX region of the proteinA gene (spa typing) as described.25 For spa typing, sequences

were analyzed using eGenomics software (http://tools.ege-nomics.com). Ridom database equivalents were identifiedusing the Ridom Spaserver website (http://www.spaserver.ridom.de). eGenomics spa types are reported using a numericalsystem (i.e. spa type 539) while Ridom spa types are reportedusing a numerical system preceded by a “t” (i.e. spa t034).Real‐time PCR was used to detect the lukF and lukScomponents of the Panton‐Valentine leukocidin (PVL) usingPVLSC‐F (50‐GCTCAGGAGATACAAG‐30) and PVLSC‐R(50‐GGATAGCAAAAGCAATG‐30) primers.26

MRSP Characterization

MRSP isolates were characterized by sequence analysis of themec‐associated direct repeat unit (dru typing),27 with drurepeats and types assigned by the Dru‐typing.org database(http://www.dru‐typing.org/search.php).

Statistical Analysis

MRS contamination rate data were described. Univariableexact conditional logistic regression was used to determine ifposition in hospital, type of clothing (SWC, LWC, or SS),animal contact, laundering location, perception of cleanliness,length of time worn, and whether clothing was worn fromhome were significant risk factors for MRSA or MRSPcontamination with significance set at P < .05. For anysignificant risk factor, odds ratio and 95% CIs were calculated.Statistical analysis was performed using software (SASOnlineDoc 9.2, SAS Institute, Inc., Cary, NC). P < .05 wasconsidered significant.

RESULTS

One‐hundred fourteen articles of hospital clothing (WC, SS)from 109 individuals were sampled; 77 WC (29 LWC, 48SWC) and 37 SS were sampled. Methicilin‐resistant staphylo-cocci (MRS) were isolated from 20 (17.5%) samples, MRSPfrom 16 (14.0%), and MRSA from 4 (3.5%). MRS were notisolated from negative controls.

Technicians were 9.5� (OR ¼ 0.95, 95% CI: 1.2–1,P ¼ .03) more likely than students to have clothing contami-nated with MRSA (Table 1). No risk factors were identified forMRSP or for overall MRS contamination.

Two MRSA isolates were identified as spa type 8/t008, aclonal complex 8 strain28 and 2 were identified as spa type 398/t034.28 Fifteen of 16 MRSP isolates were identified as dru type9a, typically associated with sequence type (ST) 71 and 1isolate was identified as a novel dru type, dt11bl.29

DISCUSSION

We found a relatively high prevalence of MRSP and MRSAcontamination of hospital clothing in a veterinary teaching

644 Veterinary Surgery 42 (2013) 643–648 © Copyright 2013 by The American College of Veterinary Surgeons

Methicillin‐Resistant Staphylococcal Contamination of Clothing Singh et al.

hospital. Hospital clothing is designed to prevent contamina-tion of the wearer’s skin or underlying clothes but may alsoserve as a source of pathogen exposure and transmission inveterinary hospitals. Furthermore, hospital clothing canpotentially act as a bridge between the veterinary hospitaland the community if contaminated clothing is taken home.The clinical and zoonotic relevance of hospital clothingcontamination is unknown, but cannot be dismissed.

In human medicine, white coats and surgical scrubs havebeen shown to harbor potentially pathogenic organisms.13–19

These studies have shown that the location of maximalcontamination occurs at the cuffs and pockets which are theareas of greatest hand contact.13,14 The contamination ratenoted here is similar to corresponding human studies.13,14,17,18

Great efforts have been made in human and veterinarymedicine to improve hand hygiene; however, post‐handhygiene contamination could still occur if hospital clothing

was handled after appropriate hygiene practices or patientscould be exposed to MRS from the clothing of veterinarypersonnel in the absence of hand contamination.

MRSA and MRSP have emerged as important pathogensin companion animals and are challenging to treat because oftheir multi‐drug resistance. MRSA is a critically importanthuman pathogen and a leading cause of hospital‐acquiredinfections in people. MRSA is also a pathogen in dogs and cats,and hospital‐acquired transmission can occur.1,5 Transmissionof MRSA between veterinary personnel and patients is aconcern in veterinary facilities, with both animal health andzoonotic implications. Zoonotic risks with MRSP are muchless than for MRSA, but human infection has been reported.5–9

MRSP is an important animal health concern because of therapid international spread of this pathogen and its leading rolein skin and soft tissue infections.2,4,5 At our hospital, MRSP isthe most common cause of surgical site infections.30

Table 1 MRSA and MRSP Contamination Rates of Hospital Clothing in a Veterinary Teaching Hospital

n MRSA MRSP Combined

PositionFaculty 6 0 1 (16.7%) 1 (16.7%)House officer 15 0 4 (26.7%) 4 (26.7%Student 59 0 8 (13.6%) 8 (13.6%)Technician 34 4 (11.8%) 3 (8.8%) 7 (20.6%)Total 114 4 (3.5%) 16 (14.0%) 20 (17.5%)

P ¼ .03 P ¼ .42 P ¼ .65Type of clothingLong WC 29 1 (3.5%) 5 (17.2%) 6 (20.7%)Short WC 48 0 7 (14.6%) 7 (14.6%)SS 37 3 (8.1%) 4 (10.8%) 7 (18.9%)Total 114 4 (3.5%) 16 (14.0%) 20 (17.5%)

P ¼ .12 P ¼ .79 P ¼ .82Animal contactYes 99 4 (4%) 16 (16.0%) 20 (20.2%)No 15 0 0 0Total 114 4 (3.5%) 16 (14.0%) 20 (17.5%)

P ¼ .65 P ¼ .12 P ¼ .07LaundryHome 22 1 (4.6%) 3 (13.6%) 4 (18.1%)Hospital 91 3 (3.3%) 13 (14.3%) 16 (17.6%)Total 113 4 (3.5%) 16 (14.2%) 20 (17.7%)

P ¼ 1.0 P ¼ 1.0 P ¼ 1.0Perception of cleanlinessClean 42 0 6 (14.3%) 6 (14.3%)Moderately cean 64 4 (6.25%) 9 (14.1%) 13 (20.3%)Dirty 8 0 1 (12.5%) 1 (12.5%)Total 114 4 (3.5%) 16 (14.0%) 20 (17.5%)

P ¼ .2 P ¼ 1.0 P ¼ .64Length of time worn<3 Days 96 4 (4.2%) 12 (12.5%) 16 (16.7%)<7 Days 11 0 3 (27.3%) 3 (27.3%)<2 Weeks 2 0 0 0>2 Weeks 4 0 1 (25%) 1 (25%)Total 113 4 (3.5%) 16 (14.2%) 20 (17.7%)

P ¼ 1.0 P ¼ .57 P ¼ .84Clothing worn from homeYes 16 0 3 (18.8%) 3 (18.8%)No 98 4 (4.1%) 13 (13.4%) 17 (17.4%)Total 114 4 (3.5%) 16 (14.0%) 20(17.5%)

P ¼ .64 P ¼ .70 P ¼ 1.0


Singh et al. Methicillin‐Resistant Staphylococcal Contamination of Clothing

Accordingly, the large percentage of hospital clothingcontaminated with MRSP (14%) is most worrisome from ananimal health perspective.MRSP is muchmore likely to spreadamongst animals, especially dogs, and has the ability to remaincolonized in dogs for long periods of time creating potentialreservoirs for infection in the hospital and community.2,4–6

No risk factors were identified for MRSP contamination,although more in depth information was not obtained becauseof the preliminary nature of the study and the difficulty inobtaining clear information about animal and environmentalcontacts before sampling. Although contact with an animal wasnot found to be a risk factor for hospital clothing contaminationwith MRS in our study, it is interesting that all 20 positivesamples were obtained from participants noted to have contactwith a patient and no positive samples were obtained fromclothing that was not in contact with a patient. Further study ofMRSP contamination, ideally with more clothing history datais needed. Technician clothing was over‐represented forMRSA contamination. The reason for this is unclear. Differ-ences in the degree of patient contact certainly exist betweentechnicians and other personnel, but why a difference would befound for MRSA but not MRSP is unclear.

Fifteen of 16 MRSP isolates were identified as dt9a and isassociated with ST 71.29 ST 71 is one of the most commonclonal lineages found in North America.29 The remainingMRSP isolate has not been identified previously.29 MRSAtyping results were somewhat unexpected. Two clones wereidentified, a clonal complex 8 spa type and the livestock‐associated spa t034. The USA100/CMRSA‐2 clone haspredominated in horses and people in previous reports ofMRSA in this region31–33 but those are older studies. ActiveMRSA surveillance of dogs and cats is not performed at ourhospital and MRSA infections are rare, so there is limitedinformation about predominant strains currently present in, orentering, OVCHSC.

While less common than USA100, clonal complex 8MRSA has been reported in dogs, and it is also common inhorses31–33 and people with horse contact33,34, and has beenfound in the environment in veterinary hospitals23,35 suggest-ing multiple possible sources of contamination. The finding ofthe livestock‐associated t034 strain was somewhat unexpectedbecause this strain is rare in domestic animals; however, thisstrain has been identified in dogs in the province36, as well as inthe environment in human hospitals.37 As a strain that typicallylacks many virulence factors38 and which is considered lessvirulent and transmissible than other endemic MRSA strains inhumans39 it is possible that this strain could be circulating incompanion animals in the absence of disease. Further, whereast034 colonization is common in pig farmers and veterinar-ians40,41, colonization rates of people in the general populationin Ontario are probably low but not adequately investigated.The nature of the sampling precluded retrospective investiga-tion of whether any patients handled by people withcontaminated lab coats had contact with livestock or whetherpersonnel themselves had contact with livestock outside of thisfacility.

To reduce costs, many human hospitals are allowingpersonnel to launder their clothing at home.16,19 Recent studies

have expressed concerns about the laundering abilities ofdomestic washing machines and Nordstrom et al.16 foundsignificantly fewer bacteria on hospital‐laundered than onhome‐laundered scrubs. In the present study, 22/113 (19.5%)samples were obtained from clothing laundered at home. Anassociation between MRS contamination and home launderingof hospital clothing was not found. However, what may be ofgreater concern is that these pieces of clothing were most likelyworn from the OVCHSC to home. Hospital‐contaminatedclothing could therefore result in exposure of householdmembers, both human and animal, to hospital‐acquiredpathogens.

Hospital infection control protocols pertaining to chang-ing of protective clothing are rather vague, indicating the needto change clothing regularly and whenever soiled; however,visibly clean does not mean pathogen‐free. We did not find anassociation between perception of cleanliness by participantsandMRS contamination. Contamination of hospital clothing inhuman hospitals has been shown to occur within hours ofdonning19 and the frequency of clothing changes is animportant risk factor for contamination in human hospitals.14

Contamination rates were higher in hospital clothing changedevery 2 days compared with that changed every day.14 In ourstudy, most participants indicated they had been wearing theirclothing for <3 days, however, an association between lengthof time worn and MRS contamination was not found. Therelationship between the frequency of hospital clothingchanges and MRS contamination requires further study.

This cross‐sectional study has several limitations. Al-though a standardized sampling technique for the recovery ofbacteria from inanimate objects in a hospital environment doesnot exist, we may have underestimated the level of MRScontamination of hospital personnel clothing. We chose to useelectrostatic cloths for recovery of bacteria from the clothing ofhospital personnel because they represent an inexpensive andsimple to use alternative to contact plates or cotton swabs thatmay offer advantages in sensitivity because of an ability toeasily sample greater surface areas and irregular surfaces.However, the sensitivity of bacterial recovery using any ofthese techniques is unknown. Another factor in potentialunderestimation of MRS contamination level was that we didnot sample the entire piece of clothing, but only the areaspreviously shown to have the highest levels of contamination(lapels, cuffs and chest pockets of LC and the umbilical regionof SS).13 Risk factor evaluation was limited as a result of thesmall number of MRS isolates recovered. A study with a largersample size is required to further evaluate for risk factors forMRS contamination of hospital clothing with appropriatestatistical power. Furthermore, longitudinal sampling would beinteresting to determine the persistence of contamination onhospital clothing. A final limitation was that a control groupwith unworn LC and SS was not included in our study.

We found a high level of MRS contamination of clothingworn by hospital personnel in a veterinary teaching hospital.MRSA andMRSP have emerged as leading causes of hospital‐acquired infections in companion animals and efforts to reducetheir transmission in the hospital environment must beimplemented. Whether hospital clothing plays a role in



transmission of MRS to patients is not fully known andrequires further investigation. Regardless, it should berecommended that hospital personnel change clothing dailyor immediately following soiling or staining, use a disposableapron when working on patients known to be carriers of MRSor have MRS‐associated infections and discourage wearingclothing to and from home.

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