Multidrug-resistant organisms such as methicillin-resistant Staphylococcus aureus (MRSA) can be spread from person to person in hospitals and long-term care facilities (LTCFs). Reference Thakur, Alhmidi and Cadnum1 Colonized patients often shed pathogens during procedures and care activities in their rooms, resulting in contamination of personnel, surfaces, and portable equipment. Reference Roghmann, Johnson and Sorkin2,Reference Alhmidi, Cadnum and Koganti3 Although most studies have evaluated contamination inside hospital and LTCF rooms, shedding of pathogens has also been demonstrated in outpatient clinics and during activities outside patient rooms. Reference Jury, Sitzlar and Kundrapu4–Reference Gontjes, Gibson, Lansing, Cassone and Mody6 However, the frequency and routes of pathogen shedding during activities outside patient rooms is not well defined. Therefore, we examined the transfer of MRSA and 2 viral surrogate markers to surfaces outside rooms by MRSA-colonized LTCF residents. Because the clothing of MRSA-colonized patients is often contaminated, Reference Kanwar, Cadnum, Thakur, Jencson and Donskey7 we hypothesized that both hands and clothing of MRSA-colonized LTCF residents contribute substantially to transfer.
Methods
We conducted a cohort study of a convenience sample of 10 MRSA-colonized residents of a 150-bed LTCF. At the time of the study, 25 MRSA-colonized residents were in the facility. Residents were excluded if they were not ambulatory or had cognitive impairment. The facility’s institutional review board approved the study protocol.
BBL culture swabs (Becton Dickinson, Sparks, MD) were used to sample the anterior nares and replicate organism detection and counting (RODAC) plates containing BBL CHROMagar with cefoxitin 6 µg/mL were used to sample hands and clothing. A 2-mL inoculum containing 1 µg cauliflower mosaic virus DNA marker and 9 log10 plaque-forming units (PFU) of bacteriophage MS2 was applied to the participant’s bedrail, bedside table, and television remote control. The DNA marker and bacteriophage MS2 were prepared as previously described. Reference Alhmidi, John and Mana8
Participants were observed during activities outside their rooms for 2–4 hours after inoculation of the surrogate markers and during appointments and activities outside their rooms for 3 days. Interactions with surfaces were classified as contact by hands, contact by clothing, or indeterminate if hands and clothing contacted a surface. Contact sites were sampled using RODAC plates and BBL culture swabs. The entire surface of small contact sites was sampled; for large surfaces, 5-cm × 10-cm areas were sampled, prioritizing sites of observed direct patient contact.
Swabs and RODAC plates were processed for recovery of MRSA. Reference Roghmann, Johnson and Sorkin2 To assess relatedness of MRSA isolates from surfaces and the nares or skin of residents, spa typing was performed. Reference Roghmann, Johnson and Sorkin2 For detection of bacteriophage MS2 and the DNA marker, the swabs were processed as previously described. Reference Alhmidi, John and Mana8
We assessed the frequency of transfer of MRSA and the surrogate markers to surfaces. The Fisher exact test was used to compare the frequencies of transfer of MRSA by culture-positive versus culture-negative participants and by hands versus clothing. The Wilcoxon rank-sum test was used to compare MRSA colony-forming units (CFU) transferred via hands versus clothing. Data were analyzed using R version 3.5.0 software (The R Foundation for Statistical Computing, Vienna, Austria).
Results
Of 10 participants, 6 had positive MRSA cultures of nares, hands, and clothing, 1 had positive hand cultures but negative nares cultures, and 3 had negative cultures from all sites. Overall, 87 sets of cultures were collected during 47 appointments or activities.
Figure 1 shows the appointments and/or activities and frequencies of recovery of MRSA and the markers. Of 87 sites sampled, MRSA, bacteriophage MS2, and the DNA marker were recovered from 27 sites (31%), 13 sites (15%), and 35 sites (40%), respectively. For all participants, 1 or both surrogate markers were recovered from at least 1 surface. MRSA was recovered from 26 (41%) of 41 sites contacted by the 7 participants with positive nares and/or hand cultures for MRSA vs 1 (4%) of 23 sites contacted by the 3 participants with negative nares, hand, and clothing cultures (P < .0001). In addition, 3 spa types (t002, t211, and t008) were recovered from the nares and/or hands of the 7 residents with MRSA nares and/or hand contamination. Isolates with matching spa types were recovered from 1 to 5 sites for each of these residents. Overall, 20 (80%) of 25 environmental MRSA isolates had spa types matching concurrent nasal or hand isolates.
Appointments and activities where cultures were collected and sites of recovery of methicillin-resistant Staphylococcus aureus (MRSA), bacteriophage MS2, and a viral DNA surrogate marker for 10 participants with MRSA colonization. The appointments included physical therapy (n = 10), hemodialysis (n = 4), and ophthalmology (n = 2). The activities included dining area (n = 24), activity area (n = 5), kitchen (n = 1), and coffee shop (n = 1).

Of 64 sites sampled for the 7 participants with positive nares and/or hand cultures, 20 (31%) involved only hand contact, 17 (27%) involved only clothing contact, and 27 (42%) involved indeterminate contact by hands and/or clothing. For hands versus clothing contact, we detected no significant differences in the percentages (6 of 20 [30%] vs 6 of 17 [35%]; P = .74) or mean CFU values (4.4 vs 1.5; P = .14) of MRSA recovered.
Discussion
We found that MRSA-colonized LTCF residents frequently disseminated MRSA and viral surrogate markers to surfaces outside their rooms. Such contamination could be an underappreciated source of pathogen transmission in LTCFs where residents often contact surfaces in shared spaces. Reference Pineles, Perencevich and Roghmann9 Patient hand hygiene could be useful to reduce dissemination of pathogens. Reference Gagné, Bédard and Maziade10 However, because both hands and clothing contributed substantially to transfer of MRSA, successful interventions may require targeting patient hand hygiene and clothing contamination.
Our study has several limitations. The study population included only men from a single facility. We did not collect information on the frequency of bathing, clothing change, or hand hygiene by participants. We do not have definitive evidence that MRSA recovered from surfaces was deposited by participants because it was not feasible to disinfect surfaces prior to contact, and spa typing is not highly discriminatory. However, MRSA was rarely recovered from sites contacted by the 3 participants with negative nares, hand, and clothing cultures, and a point-prevalence culture survey of common areas in the LTCF recovered MRSA from only 2 (3%) of 60 sites.
Acknowledgments
We thank the nursing staff at the Cleveland VA Medical Center for helpful discussions regarding potential routes of pathogen transmission.
Financial support
This work was supported by the Department of Veterans’ Affairs (Merit Review grant no. CX001848 to C.J.D).
Conflicts of interest
C.J.D. has received research grants from Clorox, PDI, and Pfizer. All other authors report no conflicts of interest relevant to this article.
