Discussion

Patient colonization and environmental contamination with multidrug-resistant organisms are common in LTCFs. In most nursing homes, approximately 50% of residents are colonized with MDROs of clinical and public health significance. ^{Reference Mody, Foxman and Bradley4,Reference McKinnell, Miller and Singh5} The high prevalence of EIP among residents in LTCF likely represents the most common source for contamination of EIP on environmental surfaces. ^{Reference McKinnell, Miller and Singh5} Our data as well as other studies ^{Reference McKinnell, Miller and Singh5} demonstrate that environmental surfaces can be a reservoir and source for EIP as environmental surfaces in resident rooms and common areas are commonly contaminated with EIP. ^{Reference McKinnell, Miller and Singh5}

Contaminated environmental surfaces and noncritical patient care items play an important role in the persistence and transmission of several key healthcare-associated pathogens including MRSA, VRE, Acinetobacter, norovirus, Pseudomonas aeruginosa, and C. difficile. ^{Reference Weber, Anderson and Rutala6} More recently, environmental contamination has been demonstrated to be associated with transmission of Ebola, mpox and Candida auris. ^{Reference Weber, Rutala and Sickbert-Bennett7}

All of these pathogens are capable of surviving in the environment for days to weeks (in some cases [C. difficile spores] months), frequently contaminate the environmental surfaces in rooms of colonized or infected patients, transiently colonize the hands and/or gloves of healthcare personnel, which may lead to transmission by healthcare personnel, and cause outbreaks in which environmental transmission was deemed to play a role. ^{Reference Weber, Anderson and Rutala6,Reference Weber, Rutala, Anderson and Sickbert-Bennett8} Importantly, a study by Stiefel et al. demonstrated that contact with the environment was just as likely to contaminate the hands of healthcare providers as was direct contact with the patient. ^{Reference Stiefel, Cadnum and Eckstein9} Studies have also shown a significant association between microbial burden and HAI risks. ^{Reference Salgado, Septowitz and John10,Reference Rutala, Kanamori and Gergen11} Further, admission to a room in which the previous patient had been colonized or infected with MRSA, VRE, Acinetobacter spp. or C. difficile, has been shown to be a significant risk factor for the newly admitted patient to develop colonization or infection. For example, the risk of acquiring C. difficile infection (CDI) after admission to a room where the prior occupant was without CDI was 4.6%, whereas 11.0% if the prior occupant had CDI. ^{Reference Shaughnessy, Micielli and DePestel12} This infection risk from the prior occupant may be less common in nursing homes than hospitals due to the longer duration of stay of the residents, but the infection transmission factors (eg, environmental contamination, hand contamination, environmental survival, suboptimal disinfection) are present. Lastly, improved terminal cleaning and disinfection of rooms ^{Reference Donskey13} as well as “no touch” room decontamination methods ^{Reference Weber, Rutala, Anderson and Sickbert-Bennett8,Reference Donskey13} has led to a decreased rate of infection in patients subsequently admitted to the room where the prior occupant was colonized or infected with an EIP. Unfortunately, “no touch” room decontamination technologies may not be attainable (eg, financial restrictions, inadequate staffing) to most LTCF. Thus, surface disinfection of noncritical environmental surfaces and medical devices (defined as those that contact intact skin) is one of the important infection prevention strategies to prevent pathogen transmission. ^{Reference Rutala and Weber14}

This infection risk from environmental surfaces is not surprising as multiple studies have demonstrated that environmental surfaces and objects in rooms are frequently not properly cleaned and disinfected. ^{Reference Donskey13,Reference Rutala and Weber14} Our data in LTCFs demonstrated that EIP were recovered from many environmental surfaces to include the bathroom floor, bed rail, over-the-bed table, sink, and chair. MRSA (3,099 MRSA CFUs) and C. difficile (863 C. difficile CFUs) were most commonly recovered from environmental surfaces in resident rooms and common areas. Sixty-five percent of resident rooms and 50% of common rooms were contaminated with at least one EIP (Table 3), which is similar to other investigations. ^{Reference McKinnell, Miller and Singh5} Approximately 11% (96/861) of the Rodac samples from resident rooms were positive for EIP (mostly C. difficile [34] and MRSA [51]), and 6.6% (28/420) of the Rodac samples from community rooms were positive for EIP (eg, C. difficile [5] and MRSA [15]). Gontjes et al found a higher rate of MDRO contamination (13.4%) of high-touch common area and rehabilitation gym surfaces in nursing homes. ^{Reference Gontjes, Gibson, Lansing, Cassone and Mody15} Other investigators found a prevalence of 28.6% (74/259) of MRSA on environmental surfaces from nursing homes in Ohio. ^{Reference Cheatham, Thapalya and Taha16}

This environmental surface contamination facilitates transfer from surfaces to residents via healthcare providers’ hands from resident contact or by residents touching contaminated environmental surfaces. A resident could also become colonized by self-inoculation by direct contact with a contaminated environmental surface. In fact, Patel et al. found that contamination of the patient room environment correlates with patient colonization in postacute care facilities ^{Reference Patel, Mantey and Mody17} and Cassone et al. identified environmental panels as a proxy for patient colonization. ^{Reference Cassone, Mantey and Perri18}

Surfaces are not regularly disinfected in healthcare facilities (including LTCFs), and these surfaces may be important in transmission of healthcare-associated pathogens. For example, a recent study found that the overall cleaning rates for environmental surfaces in LTCFs was 42% for all surfaces and 49% for high-touch surfaces and the cleaning duration was 13.6 minutes. ^{Reference McKinley, Goedken and Balkenende19} Despite the limitations of evidence in LTCFs, it is clear that EIP are commonly present on environmental surfaces, the frequency and thoroughness of cleaning and disinfection in LTCFs is suboptimal, and improvements in surface disinfection are needed in LTCFs to deliver the safest possible health care.

While the levels of EIP on environmental surfaces varied, some patient’s rooms were heavily contaminated. In addition, if a resident was labeled by the facility as colonized with an EIP, we only found that EIP in 30% of the rooms. This mismatch of EIP reported for residents versus recovered on environmental surfaces may be attributable to co-colonization. ^{Reference Donskey, Ray and Hoyen20} Frequent contact with contaminated environmental surfaces in resident rooms and common areas necessitates improved hand hygiene and daily, as well as postdischarge, environmental surface disinfection. This burden of EIP on environmental surfaces in resident rooms and common areas requires standardized and comprehensive cleaning and disinfection that address known barriers in LTCF (eg, resident present during cleaning and disinfection, semi-private rooms, remove room clutter) ^{Reference McKinley, Goedken and Balkenende19} in resident rooms and common areas. ^{Reference McKinley, Goedken and Balkenende19,Reference Thomas, Thomas, Conly and Lorenzetti21} Previous studies have demonstrated that daily disinfection of surfaces in CDI and MRSA isolation rooms reduced acquisition of the pathogens on hands after contacting high-touch surfaces and reduced contamination of hands of healthcare workers caring for the patients. ^{Reference Kundrapu, Sunkesula, Jury, Sitzlar and Donskey22}

There are limitations to this study. There was no molecular typing to match the environmental isolates with clinical isolates obtained from residents and a small number of LTCFs were studied. Additionally, since patient level risk factors for contamination were not obtained, we were not able to correlate cleaning and disinfection practices or patient medical conditions (eg, incontinent of feces) to elevated levels of environmental surface contamination.

While the mean of EIP found in for-profit LCTF was higher than non-profit LCTF, one non-profit LCTF had similar levels as the two for-profit LCTF. A higher frequency of hospitalization for infection has been reported in for-profit LCTF. ^{Reference Zimmerman, Gruber-Baldini, Hebel, Sloane and Magaziner23} We were unable to assess other potential reasons for the disparities in levels of EIP (eg, staffing levels, physical plant, etc.) as this information was not collected.

Improved cleaning and disinfection of the contaminated environmental surfaces (ie, noncritical surfaces and medical equipment) is critical to reduce the risk of EIP transmission via environmental surfaces through contact with environmental surfaces and sharing common areas in nursing homes (eg, activity rooms). Further, bundles with evidence-based components (eg, resident and staff hand hygiene promotion, environmental disinfection, enhanced barrier precautions [ie, gown, glove with high-contact resident care activities]) may be necessary to reduce the risk of MDRO transmission in LTCFs. ^{Reference Kanamori, Rutala, Sickbert-Bennett and Weber1,Reference Rutala and Weber14} Preventing healthcare-associated infection is critical for delivering safe and high-quality care in LTCFs and across the healthcare system.