Background
As the world population is aging, the number of people aged 65 and older in the United States are projected to nearly double in size from 49 million in 2016 (15% of the population) to 81 million in 2040 (22% of the population). Reference Kanamori, Rutala, Sickbert-Bennett and Weber1,Reference Vespa, Armstrong and Medina2 With the significant aging of the population, there are now over 1.7 million residents in the 16,000 US nursing homes and more people in long-term care facilities (LTCFs) than in acute-care hospitals, which highlights the importance of infection prevention in these facilities. Reference Kanamori, Rutala, Sickbert-Bennett and Weber1,Reference Sturm, Flood, Montoya, Mody and Cassone3 LTCFs, including nursing homes, skilled nursing facilities, and assisted living facilities, provide a variety of services, both medical, nursing and personal care, to people who need ongoing care over an extended period. Reference Kanamori, Rutala, Sickbert-Bennett and Weber1,Reference Sturm, Flood, Montoya, Mody and Cassone3
About 15% of nursing home residents acquire an infection and infection (eg, sepsis) is one of the top 5 causes of death in nursing homes. Reference Kanamori, Rutala, Sickbert-Bennett and Weber1,Reference Sturm, Flood, Montoya, Mody and Cassone3 This is attributable to predisposing comorbidities, severity of illness, weakened immune system, functional and cognitive impairment, frequent use of indwelling devices (eg, urinary catheter), recent hospitalization, frequent antibiotic use, potential transmission through group activities and therapeutic sessions, and difficulties in adhering to infection prevention guidelines due to multiple tasks of staff, limitation of funds, and less trained/experienced staff. Reference Kanamori, Rutala, Sickbert-Bennett and Weber1,Reference Sturm, Flood, Montoya, Mody and Cassone3
Nursing home patients have a high prevalence of colonization. In one prospective study of newly admitted patients in six nursing homes in Michigan, more than 50% (56.8%) were colonized with multidrug-resistant organisms (MDROs) at enrollment, including 16% with methicillin-resistant Staphylococcus aureus (MRSA); 33% with vancomycin-resistant Enterococcus (VRE), and 32% with multidrug-resistant Gram-negative rods (MDR-GNRs). Reference Mody, Foxman and Bradley4 The high prevalence of MDROs in nursing home residents is linked, in part, to environmental surface contamination. Reference McKinnell, Miller and Singh5 McKinnell et al. found environmental MDRO contamination in 74% of resident rooms and 93% of common areas when half of the residents harbored an MDRO. Reference McKinnell, Miller and Singh5
It has been well documented that hospital environmental surfaces play an important role in the transmission of MDROs such as MRSA and VRE. Reference Weber, Anderson and Rutala6 Since there are few studies focused on contaminated environmental surfaces in LTCFs, we conducted a quantitative analysis of the microbial burden and prevalence of epidemiologically important pathogens (EIP) found on LTCF environmental surfaces.
Methods
A convenience sample of 5 LTCF in North Carolina was studied. The LTCF operated with 57–173 beds. Microbiological samples were collected using Rodac plates (25cm Reference Vespa, Armstrong and Medina2 /plate) from resident rooms and common areas in five, North Carolina LTCFs in 2016. Each LTCF was sampled twice, separated by 2–22 days, and 30 total rooms were sampled (5 LTCFs; 4 resident rooms and 2 common rooms per LTCF). Five Rodac plates containing Dey-Engley neutralizing agar (Becton Dickinson & Company, Sparks, MD) were used per site to evaluate vegetative bacteria and five Clostridioides difficile Selective Agar plates were used per site to recover C. difficile. The DE Agar plates were incubated at 37oC for 48 hours and the C. difficile Selective Agar plates (not prereduced) were incubated anaerobically (Anaeropack; Mitsubishi Gas Chemical) at 37o for 48 hours for C. difficile. At each facility, five Rodac samples per environmental site were collected from eight different environmental surface sites from the room of an ambulatory resident (not bedridden) reported to be colonized with an EIP, as well as from a room of a resident reported to be non-colonized. The colonization status of the resident was not confirmed by the investigators (eg, by medical record review). EIP were defined as MRSA, VRE, C. difficile, and MDR-Gram-negative rods (eg, Klebsiella). When evaluating gram-negative rods (GNRs), morphologically identical GNRs per site were identified with API (Biomerieux, Durham, NC) and Kirby-Bauer antibiotic susceptibility testing was performed on GNR isolates. An MDR GNB was defined at being resistant to 3 or more major classes of antimicrobials. No molecular testing to assess for relatedness of isolates was performed. In addition, five samples per environmental site from eight different environmental surfaces (eg, floors, cabinet faces, countertops, refrigerators, chairs, tables, hand rails, etc.) were collected from two common areas in the facility. Of the 10 common areas, 6 rooms had chairs and tables and no dining, 3 had dining areas, and one room was for visiting, a library and a fish and bird room. If the intended site was not available, an alternative site was chosen. Data were analyzed for each environmental site sampled in a resident room or common area for the presence of total colony-forming units (CFU) of bacteria, the mean CFU per Rodac, the total EIP CFU by site, mean EIP CFU per Rodac and presence of at least one EIP per room. The study was approved by the UNC Institutional Review Board.
Results
Table 1 summarizes the data on total CFU and EIP CFU recovered from environmental sites by reported colonization status of the resident. Rooms of residents with reported colonization had much greater EIP CFU per Rodac (8.32, 95%CI 8.05, 8.60) than rooms of non-colonized residents (0.78, 95% CI 0.70, 0.86). If a resident was labeled by the facility as colonized with an EIP, we only found that EIP in 30% of the rooms. MRSA was the most common EIP recovered from Rodacs (3,099 CFUs), followed by C. difficile (863 CFUs) and MDR-GNR (187 CFUs). With the exception of MRSA, very few EIP were recovered from the common areas sampled at these LTCFs (Table 2).
Table 1. Total colony-forming units (CFU) and epidemiologically important pathogens (EIP) recovered from environmental sites in resident rooms, stratified by colonization status of resident, in five long-term care facilities in North Carolina
CFU, colony-forming units; EPI, epidemiologically important pathogens.
Table 2. Frequency of environmental surface contamination with epidemiologically important pathogens (EIP) in resident rooms and common rooms in five long-term care facilities in North Carolina
MDR-GNR, multidrug-resistant Gram-negative rods; MRSA, methicillin-resistant Staphylococcus aureus; VRE, vancomycin-resistant enterococci.
Sixty-five percent of the resident rooms and 50% of the common areas were positive for at least one EIP (Table 3). In resident rooms, environmental sites contaminated with EIP in greater than 15% of the samples collected were the closet door, bathroom floor, and overbed table. The floor and blackboard frame in the common rooms were contaminated with EIP ≥25% of the samples collected (Table 4). The total CFU of EIP recovered from the five LTCFs varied greatly: LTCF 1-1,462 EIP, LTCF 2-3 EIP, LTCF 3-2 EIP, LTCF 4-1,321 EIP, and LTCF 5-1,389 EIP. Some resident rooms (8/20, 40%) had substantial EIP contamination of environmental surfaces (eg, one resident room 850 CFU EIP, mostly C. difficile [848]) but 35% (7/20) had no EIP recovered and 25% (5/20) had less than 10 EIP recovered from environmental surfaces. MRSA or C. difficile was recovered from 55% (11/20) of the LTCFs resident rooms; 50% (10/20) were contaminated with MRSA; and 30% (6/20 resident rooms) were contaminated with C. difficile. Of the 861 Rodacs collected from resident rooms, 34 (4.0%), 51 (6.0%), 1 (0.1%) and 10 (1.1%) were positive for C. difficile, MRSA, VRE and MDR-GNR, respectively.
Table 3. Number of rooms in long-term care facilities with at least one epidemiologically important pathogens (EIP)
EIP, epidemiologically important pathogens; MDR-GNR, multidrug-resistant Gram-negative rods; MRSA, methicillin-resistant Staphylococcus aureus; VRE, vancomycin-resistant enterococci.
Table 4. Frequency of environmental sites positive for epidemiologically important pathogens (EIP) in resident rooms and common rooms in five long-term care facilities in North Carolina
EIP, epidemiologically important pathogens.
The characteristics of study LTCFs are displayed in Table 5. None of the study LTCFs provided care for ventilated patients. Of note, two LCRFs were for profit and three were not-for profit. The mean of EIP found on surfaces from non-profit versus for-profit LTCF was 489 versus 1325, but LCTF 1 (non-profit) had similar levels of EIP as the two for-profit LCTF (ie, 1,321 and 1,389).
Table 5. Information about studied long-term care facilities
CCRC, Continuing Care Retirement Center; LTCF, long-term care facilities.
Participates in Medicare = accepts payment/partial payment via Medicare insurance, federal health insurance for people 65 and older (medicare.gov).
Participates in Medicaid = accepts payment/partial payment via Medicaid insurance, a health insurance program for low-income individuals and families who cannot afford healthcare costs (ncdhhs.gov).
CCRC: Continuing care retirement communities, also known as CCRCs or life plan communities, are a long-term care option for older people who want to stay in the same place through different phases of the aging process. (aarp.org).
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.
Conclusions
We found varying levels of epidemiologically important pathogens on environmental sites at LTCFs. Colonization status of a resident was a strong predictor of higher levels of EIP being recovered from his/her room.
Financial support
This study was supported, in part, by the University of North Carolina Medical Center and the Statewide Program for Infection Control and Epidemiology.
Competing interests
Dr. Rutala is a consultant for Professional Disposable International (PDI) and Kinnos. Dr. Weber is a consultant for PDI and Germitec. All other authors have no disclosures.
