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Occupational risk of exposure to methicillin-resistant Staphylococcus aureus (MRSA) and the quality of infection hygiene in nursing homes

Occupational risk of exposure to methicillin-resistant Staphylococcus aureus (MRSA) and the... Front. Environ. Sci. Eng. 2021, 15(3): 41 https://doi.org/10.1007/s11783-020-1333-y RESEARCH ARTICLE Occupational risk of exposure to methicillin-resistant Staphylococcus aureus (MRSA) and the quality of infection hygiene in nursing homes 1 1 2 2 Pil Uthaug Rasmussen (✉) , Katrine Uhrbrand , Mette Damkjær Bartels , Helle Neustrup , Dorina Gabriela 1,3 1,4 1 Karottki , Ute Bültmann , Anne Mette Madsen 1 National Research Centre for the Working Environment, Lersø Parkallé 105, 2100 Copenhagen Ø, Denmark 2 Department of Clinical Microbiology, Hvidovre Hospital, Kettegård Allé 30, 2650 Hvidovre, Denmark 3 The Danish Working Environment Authority, Landskronagade 33, 2100 Copenhagen, Denmark 4 University Medical Center Groningen, Department of Health Sciences, Community & Occupational Medicine, University of Groningen, 9700 Groningen, The Netherlands HIGH LIGHTS GRAPHIC A BSTRA C T � Staff members were not colonised with MRSA. � But staff were exposed to MRSA from air, sedimented dust and surfaces. � MRSA was found in the rooms of MRSA- colonised residents but not in common areas. � Staff worry about MRSA and spreading it to other residents, family, and acquaintances. � The use of protective eyewear and facemasks could be improved. AR TICL E I N F O ABSTRA CT Article history: Methicillin-resistant Staphylococcus aureus (MRSA) is an increasing health concern across the globe and is often prevalent at long-term care facilities, such as nursing homes. However, we know little of Received 6 July 2020 whether nursing home staff is exposed to MRSA via air and surfaces. We investigated whether staff Revised 4 September 2020 members at nursing homes are colonised with and exposed to culturable MRSA, and assessed staff Accepted 7 October 2020 members’ self-reported knowledge of MRSA and compliance with infection hygiene guidelines. Five Available online 13 November 2020 nursing homes with MRSA positive residents were visited in Copenhagen, Denmark. Personal bioaerosol exposure samples and environmental samples from surfaces, sedimented dust and bioaerosols were examined for MRSA and methicillin-susceptible S. aureus (MSSA) to determine Keywords: occupational exposure. Swabs were taken from staffs’ nose, throat, and hands to determine whether they were colonised with MRSA. An online questionnaire about MRSA and infection control was Antibiotic resistance distributed. No staff members were colonised with MRSA, but MRSAwas detected in the rooms of the Airborne MRSA colonised residents in two out of the five nursing homes. MRSA was observed in air (n = 4 out of 42, Bioaerosols 3 3 2 ranging from 2.9–7.9 CFU/m ), sedimented dust (n = 1 out of 58, 1.1  10 CFU/m /d), and on Healthcare-associated infections surfaces (n = 9 out of 113, 0.04–70.8 CFU/m ). The questionnaire revealed that half of the staff Healthcare worker members worry about spreading MRSA to others. Identified aspects for improvement were improved Occupational health availability and use of protective equipment, not transferring cleaning supplies (e.g., vacuum cleaners) between residents’ rooms and to reduce worry of MRSA, e.g., through education. © The Author(s) 2020. This article is published with open access at link.springer.com and journal.hep. com.cn ✉ Corresponding author E-mail: pur@nfa.dk Special Issue—Bioaerosol, Environment and Health (Responsible Editors: Can Wang, Jungho Hwang, Jingkun Jiang & Maosheng Yao) 2 Front. Environ. Sci. Eng. 2021, 15(3): 41 members, or if staff members are colonised with MRSA 1 Introduction they can act as vectors to other residents or colleagues (Albrich and Harbarth, 2008).We therefore need i) more More than 40000 seniors (i.e. over 65 years) are currently information on the transfer of MRSA via air and surfaces residing in nursing homes in Denmark (Sundheds- Og within nursing home settings and the risks it poses for the ldreministeriet, 2016). This number is expected to increase staff, and ii) to understand the staff’s experience with in the coming years (Danmarks Statistik, 2020). In MRSA and compliance with infection hygiene guidelines. Denmark, half of the residents have one or more chronic To answer these questions five nursing homes, which had disease and over two thirds have dementia (Sundheds- Og residents colonised with MRSA were visited twice in the ldreministeriet, 2016). The residents also have an Capital Region of Denmark. Staff members were screened increased use of pharmaceuticals, are more in contact for MRSA, and bioaerosol, sedimented dust, and surface with doctors, and have more admissions to the hospital samples were taken. Furthermore, a questionnaire about than others of the same age who do not live in nursing MRSA and hygiene practices was sent to nursing home homes (Sundheds- Og ldreministeriet, 2016). These staff members in four of the nursing homes. The study factors are contributing to the typically high prevalence of aimed at answering whether MRSA is present on the hands multidrug-resistant microorganisms and MRSA in nursing and in the airways of nursing home staff, whether nursing homes (Bradley, 1999; Stone et al., 2008; Garazi et al., home staff is exposed to MRSA or MSSA during their 2009). We therefore need more information on the risk of work in both the colonised residents’ rooms and in occupational exposure to multidrug-resistant microorgan- common areas, and what the level of knowledge and isms for healthcare workers. experience of staff members to MRSA and infection Multidrug-resistant microorganisms, such as methicil- hygiene is. lin-resistant Staphylococcus aureus (MRSA), a bacterium resistant to many of the antibiotics typically used for treatment, is a worldwide concern (CDC, 2013; WHO, 2 Materials and methods 2014; DANMAP, 2018). MRSA accounts for more than half of S. aureus infections worldwide (WHO, 2014), but 2.1 Sampling location and participants in Denmark, the incidence level is low, with almost 4000 new cases in 2018 constituting only 1.6% of S. aureus Sampling was carried out from October 2017 to June 2018 bacteraemia cases (DANMAP, 2018). To avoid spread, at five nursing homes (A-E) in the Capital Region of adequate precautions have to be taken when healthcare Denmark with residents known to be MRSA-colonised. personnel are interacting with MRSA-infected or – The nursing homes were selected because they had at least colonised individuals (Calfee et al., 2014). In hospitals, one MRSA positive resident who was monitored at the this includes isolation of patients in their rooms (Calfee MRSA Knowledge Center at Hvidovre Hospital. Each et al., 2014). In Danish nursing homes, isolation of nursing home was visited on two separate occasions with residents with MRSA is not allowed unless they have a 14 days apart and 52 staff members in different job respiratory infection. In addition, rooms are rented to the functions participated in the study. A total of 79 personal residents who have some autonomy in their own rooms, exposure assessments were conducted as some staff while healthcare and cleaning personnel assist with members participated on both of the two sampling days. personal care and cleaning. Residents are fully integrated Four to eleven personal assessments were done per into everyday activities at the nursing home and in sampling day, and of the 79 assessments conducted, 8 common areas, and this may facilitate MRSA transmission (10%) were on nurses, 37 (47%) were on social and and increase the exposure of staff members in nursing healthcare assistants, 15 (19%)wereonsocialand homes when interacting directly and indirectly with healthcare helpers, 7 (9%) were on cleaning assistants, individuals colonised with MRSA. Nevertheless, little is and 12 (15%) were on staff with other job titles. known about the degree to which nursing home staff Participation was voluntary and all staff members and members are exposed to, colonised with, or infected with residents colonised with MRSA signed a consent form methicillin-susceptible S. aureus (MSSA) and MRSA, before entering the project. The resident had to give both especially in regards to airborne MRSA, which for many oral and written consent to have MRSA samples taken may be an overlooked transmission route (Kozajda et al., from the environment of their room. Ethical approval was 2019). According to the MRSA guidelines from the Danish applied for, but the National Committee on Health Health Authority, extended hygiene practices have to be Research Ethics decided an approval was not needed for met when taking care of the infected or colonised residents the types of samples taken (swabs and bioaerosol and when cleaning their room (The Danish Health measurements), as only microorganisms but not biological Authority, 2016). If adequate hygiene practices are not material was taken from the participants. met, there may be a higher risk of exposure to staff Pil Uthaug Rasmussen et al. MRSA in nursing homes 3 2.2 MRSA screening of staff sampled for 20 min at a flow rate of 3.5 L/min. In addition, stationary air sampling was performed by collecting Staff members were screened for MRSA in the nose, throat bacteria directly on SA agar using a six-stage Andersen and on their hands at the beginning and end of the working Cascade Impactor (ACI; N6, Thermo Fisher Scientific Inc. day. Sampling was done using the eSwab transport system Waltham, MA, USA) with a flow rate of 28.3 L/min (eSwab; Copan, Brescia, Italy) which consists of a flocked measuring for an average of 10 minutes and at a height of 1 nylon swab and 1 ml transport medium. Nasal samples m. ACI samples were stored in a cool box and incubated were taken from the anterior nares by rotating the same directly at 37°C for 48 h upon return to the laboratory. swabs in each nostril. Throat samples were obtained by Electrostatic dust cloths (EDCs; ZEEMAN, Alphen, swabbing the palatopharyngeal arch and tonsils on both Holland, surface exposure area of 0.0209 m (19 cm  11 sides. Hand samples were collected by rotating the eSwabs cm)) were used for long-term passive sampling of axially and laterally in a zigzag motion over the entire sedimented dust. On each sampling visit, EDCs were surface of each palm, using the same swabs on both right placed on an open surface and dust allowed to settle for 7 d. and left hand. After sampling, all swabs were transferred to EDCs were placed in the residences of the MRSA- their container, stored cold (4°C), and processed within 24 colonised individuals, common areas, corridors in com- hours of sampling. Hand samples were vortexed for 2 min, mon areas, staff changing rooms, staff offices, and laundry plated in serial-dilutions on chromogenic SaSelect agar rooms at a height ranging from 0.7–1.8 m. In total, 11–12 (SA; Biorad, Solna, Sweden) and incubated at 37°C for 48 EDCs were placed per nursing home. hours. Eswabs from nose and throat samples were An outdoor stationary reference measurement was taken inoculated into MRSA enrichment broth (TSB containing at every sampling. Outdoor references were taken with a 2.5% NaCl, 3.5 mg/L cefoxitin, and 20 mg/L aztreonam; GSP placed at a height of 1.5 m. The average sampling (Böcher et al., 2010)) and incubated overnight at 35°C. Ten time of the reference measurements was 385 min. µl of broth was then inoculated onto a selective MRSA Temperature and relative humidity were measured inside plate (Brilliance MRSA 2 agar, Oxoid, Thermo Fisher and outside the nursing homes during sampling using Scientific) and an unselective 5% Danish Blood agar plate Tinytag Plus Data Loggers (Germini Data Loggers, United and incubated overnight. Colonies suggestive of S. aureus Kingdom; Table S1). were identified using matrix-assisted laser desorption- Bacteria from all GSP filters and EDC cloths were ionisation time-of-flight (MALDI-TOF) mass spectro- extracted in 5 and 20 mL of pyrogen-free water containing metry (MS) and their susceptibility to cefoxitin (30 µg) 0.85% NaCl and 0.05% Tween 80, respectively. Staphy- was determined. For isolates resistant to cefoxitin accord- lococci bacteria were enumerated by dilution plating and ing to EUCAST breakpoints, the presence of mecAor incubation on SA agar at 37°C for 48 h. mecC was confirmed by an in-house PCR. Environmental surface sampling of armrests, tables, door handles, light switches, and TV remotes was 2.3 Exposure to MRSA conducted in the MRSA individuals’ residences and in the common areas of the nursing homes (on average 10 To collect bacteria from the inhalation zone of the nursing swabs in total of each type, both in residences and common home staff, personal air samplers (Gesamtstaubprobe- rooms), and surface samples were furthermore taken from nahme sampler (GSP), CIS, BGI Inc., Waltham, MA, the bed rails of the resident colonised with MRSA (n = 10). USA) mounted with a 37 mm polycarbonate filter (PC, Sampling was done using eSwabs by rotating the swab pore size 1.0 µm, Main Manufacturing, Grand Blanc, axially and laterally in a zigzag motion over a surface area MI, USA) and a flow rate of 3.5 L/min were used. The of approximately 100 cm . Samples were stored and personal GSP samplers, connected to pumps worn in a processed as described for the hand swabs. backpack, were placed in the breathing zone of the participants. The GSP was chosen, as it samples inhalable 2.4 Identification and molecular characterization of MRSA particles (airflow 3.5 L/min), and as it has been described isolates to have a good sampling efficiency (Kenny et al., 1999). The personal air sampling was performed during an entire Presumptive S. aureus isolates were recognized based on working day while the nursing home staff performed morphological appearance on SA media. Identification was normal job tasks. The average personal air sampling period performed on all the presumptive S. aureus isolates from was 315 min. all samples using MALDI-TOF MS as described in (Feld To collect air samples during specific work tasks, e.g. et al., 2018). All S. aureus isolates from exposure samples while providing assistance to the resident colonised with were tested for methicillin resistance by sub cultivation on MRSA or during cleaning of their residence, stationary Brilliance MRSA 2agarfor 24 hat37°C. One short-term air sampling was used. For this, a GSP sampler presumptive MRSA isolate from each sample was selected with a PC filter was placed at a fixed height of 1.5 m and for molecular verification and were confirmed to be MRSA 4 Front. Environ. Sci. Eng. 2021, 15(3): 41 by an in-house multiplex PCR targeting the genes mecA, 2.6 Data and statistical analyses mecC, nuc and femA. MRSA isolates were then whole genome sequenced on an Illumina MiSeq and assembled Bacterial concentrations were calculated as geometric 3 3 mean (GM) concentration per m of air (CFU/m ) for as previously described (Bartels et al., 2015). cgMLST was GSP and ACI air samples, as GM concentration per m per performed using the Ridom SeqSphere software and the day (CFU/m /d) for EDC samples, as GM concentration isolates were compared to the whole genome sequenced 2 2 per cm (CFU/cm ) for surface samples, and GM isolates from the MRSA colonised patients from the concentration per hands (CFU/hands) for hand samples. specific nursing home in order to confirm whether the Limits of detection was on average: personal GSP = 8.2 environmental MRSA was identical to the isolate of the 3 3 CFU/m , GSP during tasks = 47.6 CFU/m , ACI during patient. 3 2 tasks = 2.9 CFU/m , EDC = 91.1 CFU/m /d, eSwabs were 0.04 CFU/cm for surfaces and 8.3 CFU/ hands for hand 2.5 Questionnaire swabs. A self-administered questionnaire was distributed among In order to investigate the impact of nursing home and the staff members of four nursing homes (A, B, C, E) job group on responses to the questionnaire, we ran linear covering approximately 100 questions on knowledge mixed effect models with nursing home, job and their regarding MRSA and infection hygiene. Due to time interaction as fixed effects. For questions where respon- constraints at the nursing home, staff members at nursing dents had to give a rating of e.g. their knowledge, the home D did not participate. The questionnaire inquired answers were given on a scale from 1–5, and otherwise about the participant’s background, knowledge of and answers were treated as categories. All analyses were experience with MRSA and infection hygiene, compliance conducted in R v.3.5.3 (R. Core Team, 2019), using with infection hygiene guidelines, and opinions on the packages lme4 v. 1.1–24 and car v. 3.0–3 (Fox and consequences of working with residents with MRSA. The Weisberg, 2011; Bates et al., 2014). questionnaire was sent to 161 nursing home staff members, and 74 respondents answered the questionnaire (46% 3 Results response rate). Both complete (n = 51) and partial (n = 23) completions were included in the analyses. Due to the 3.1 Exposure to MRSA length of the questionnaire, we only report key findings in the Results section, but a full description can be found in MALDI-TOF identification was attempted on bacterial the Supplementary Information (Results S1, Tables S2– isolates from the stationary ACI air samples, stationary and S6). Table 1 Staphylococcus aureus and methicillin-resistant S. aureus (MRSA) found during screening of staff members and the exposure to MRSA in air, surface and sedimented dust samples. Percentages calculated based on the total number of samples S. aureus positive samples MRSA positive samples Total number Sample group of samples % n Concentration % n Concentration MRSA screening of staff –– 158 00 Nasal swab –– 156 00 Throat swab 158 10.8 17 10–150 CFU/hand 0 0 Hand swab 472 3.6% 17 0 0 Total of all screening samples Exposure to MRSA 79 15.2 12 7.3–201.9 CFU/m 00 Personal GSP air sample 46 6.5 3 285.7–1857.1 CFU/m 00 Stationary GSP air sample 3 3 42 21.4 9 2.9–173.1 CFU/m 9.5 4 2.9–7.9 CFU/m 6-stage ACI stationary air sample 2 3 2 58 8.6 5 91.1–1093.6 CFU/m /d 1.7 1 1.1  10 CFU/m /d EDC sedimented dust sample 2 2 113 23.6 26 0.04–70.8 CFU/cm 8.2 9 0.04–70.8 CFU/cm Surface sample Total of all exposure samples 338 16.3% 55 4.1% Stationary GSP outdoor air reference 10 0 0 0 Staff members were screened for MRSA at the start and end of the working day. Incidence of S. aureus was not determined for nasal and throat samples. ACI = stationary six-stage Andersen Cascade Impactor, GSP = stationary Gesamtstaubprobenahme sampler, EDC = electrostatic dust cloth. Each 6-stage ACI stationary air sample was grown on six chromogenic SaSelect agar plates, but here all six plates are presented as one sample. Pil Uthaug Rasmussen et al. MRSA in nursing homes 5 personal GSP air samples, outdoor reference air samples, whereas MSSA was detected in all sample types and in surfaces samples, and hand swabs. In total, 423 S. aureus both the common areas and in the residences. MRSA was isolates were identified, and these were found in 72 out of found during specific work tasks: during personal care the 496 samples examined for S. aureus (Table 1). Of the S. tasks, cleaning of floors, and in the background air aureus isolates, 25.3% (107 isolates) were presumed to be measurements (Table 2). MRSA was observed in particles methicillin resistant. These MRSA isolates were found in a in the size range of 4.7 µm and above. total of 14 samples, consisting of 4 stationary ACI air MSSA was found on surfaces both in common areas and samples, 1 EDC sample, and 9 surface samples (Table 1). the colonised residents’ room (Table 3). However, MRSA MRSAwas not detected in nose, throat or hand swabs from was only detected in the room of the resident colonised the staff members (neither at the beginning nor at the with MRSA on armrests, bed rails, TV-remotes, and on the end of the working day), in any of the stationary or door handles (Table 3). personal GSP air samples, nor in references air samples (Table 1). 3.2 Knowledge of MRSA and infection hygiene Overall, MRSA was detected in the colonised-residents’ room but not in common areas, and while MSSA was The majority of respondents (97% and 77%, respectively) present at all nursing homes, MRSA was only detected in had heard of and reported their knowledge about MRSA as two of the five nursing homes. Whole genome sequencing good, very good or excellent (Figs. 2(a)–2(b)), however, showed that the MRSA spa types (t) and multilocus knowledge of MRSA differed among job groups (F = 6,42 sequence types (ST) (t3841/ST672 and t223/ST22) found 3.67, P = 0.008; Fig. 2(c)). Most respondents (83%) at each nursing home matched that of the infected resident similarly rated their knowledge of infection hygiene as at that home (Fig. 1). good, very good or excellent (Fig. 3(a)), though this again differed among job groups (F = 3.67, P = 0.029; Fig. 3 6,49 (b)). Thirty-eight percent of respondents had heard of but not read the ‘Guideline for prevention of spread of MRSA’ from the Danish Health Authority, and 21% had not heard of it. Ninety percent reported that they always or mostly always followed the infection hygiene guidelines, but this differed among job groups and nursing homes (a significant interaction effect; F = 2.14, P = 0.039). 12,36 Eighty-one percent reported that their workplace as a whole always or almost always followed the guidelines. The majority of the respondents reported easy access to personal protective equipment such as gloves and protective clothing. However, protective eyewear (incl. visors) and facemasks (surgical masks and respirators) seemed to be less easily available. Around 40% and 10% of the respondents reported that they did not have easy access to protective eyewear and facemasks, respectively. The level of easy access differed among nursing homes (protective eyewear: F = 2.27, P = 0.097; facemasks: 3,36 F =7.94, P< 0.001). For staff with care tasks, 3,36 facemasks was used most of the time when there was a risk of splashes and sprays of bodily fluids, however a large group (19%) stated that they never use it. Similarly, 50% said they never use protective eyewear in similar situations. Cleaning supplies (e.g., vacuums) sometimes gets transferred from the MRSA residents’ room to other Fig. 1 Whole genome clustering of methicillin-resistant S. places of the nursing home (15% state it always happens aureus (MRSA) isolates at the two nursing homes (a) and and 8% that it sometimes happens). Respondents reported (b) were MRSA was detected. MRSA isolates starting with M is that they are a lot or very much (30%) worried about from the colonised residents, while isolates starting with WGS are contracting MRSA, a lot or very much (49%) worried from surface and air samples collected at the nursing home. about bringing MRSA from work to family and acquain- tances, and a lot and very much (45%) worried about being Air and sedimented dust samples showed that the the cause of transfer of MRSA to other residents in the nursing home staff members were exposed to MRSA in the nursing home. Whether contracting MRSA would have a air of the MRSA-colonised resident’s room (Table 1–2), negative influence on respondents’ social lives, 52% 6 Front. Environ. Sci. Eng. 2021, 15(3): 41 Table 2 Potential exposure to Staphylococcus aureus and methicillin-resistant S. aureus (MRSA) in air samples during specific work tasks conducted in the room of the MRSA-colonised resident. Shown are samples positive for S. aureus and MRSA S. aureus positive samples MRSA positive samples Total number of Work task GM Range GM Range samples n n 3 3 3 3 (CFU/m ) (CFU/m ) (CFU/m ) (CFU/m ) ACI Personal care 6 21.1 8.9–56.5 2 7.9 – 1 Cleaning of surfaces & fomites 9 134.3 – 1- – 0 Cleaning of floors 6 4.8 3.5–7.9 3 5.6 3.9–7.9 2 –– –– Bed making 2 0 0 –– –– Nursing tasks 2 0 0 Background; MRSA residence 8 22.6 2.9–173.1 2 2.9 1 Background; Common area 9 3.5 – 1 – 0 GSP – –– Personal care 9 285.7 1 0 – –– 0 Cleaning of surfaces & fomites 5 – 0 – –– 0 Cleaning of surfaces, fomites & floor 4 1857.1 1 –– –– 0 Cleaning of floors 4 0 –– –– 0 Bed making 2 0 –– –– 0 Nursing tasks 2 0 –– –– Other (marking of clothes) 1 - – –– 0 Background; MRSA residence 8 571.4 1 –– –– 0 Background; common area 11 0 –– –– Outdoor GSP reference 10 0 0 Geometric means (GM), ranges, and number (n) of positive S. aureus and MRSA samples. A hyphen is listed where no positive samples were observed or for ranges when only one positive sample was found. ACI = stationary six-stage Andersen Cascade Impactor, GSP = stationary Gesamtstaubprobenahme sampler. Values from ACI samples are sums of all the six stages. Table 3 Surface samples found positive for Staphylococcus aureus and methicillin-resistant S. aureus (MRSA) in the residences of the MRSA- colonised individuals and in the common areas of the nursing homes Residence of MRSA-colonised individual Common area S. aureus MRSA positive S. aureus MRSA positive positive samples samples positive samples samples Sampling point Number of Number of GM GM GM GM samples samples % n (CFU % n (CFU % n (CFU/ % n (CFU/ 2 2 2 2 /cm ) “/cm ) cm ) cm ) Armrest 10 30 3 0.53 30 3 0.33 10 30 3 0.19 0 0 Table 10 10 1 1 0 0 – 10 30 3 0.37 0 0 Door handle 11 18 2 8.28 9 1 5.33 12 42 5 0.88 0 0 – – Light switch 10 10 1 0.24 0 0 – 10 0 0 00 – – TV remote 10 30 3 0.49 20 2 0.19 10 0 0 00 –– – – – – Bed rail 10 40 4 3.63 30 3 3.07 0 As beds are only located in residents’ rooms, no bed rail samples were taken from common areas. answered that they agreed or completely agreed, however 4 Discussion this depended on both nursing home and job group (F = 3,29 3.05, P = 0.044; F = 2.50, P = 0.045), where 6,42 Our study showed that staff members working in nursing respondents from two of the nursing home mainly reported homes in The Capital Region of Denmark were not they neither agreed nor disagreed, but respondents from the colonised with culturable MRSA, similar to findings in two other nursing homes were mainly more worried. Stockholm, Sweden (Andersson et al., 2012) where no Pil Uthaug Rasmussen et al. MRSA in nursing homes 7 Fig. 3 Self-reported knowledge of infection hygiene. Shown are a) how respondents assess their knowledge, and b) how their average self-assessed knowledge differs among job groups. Nurses have the longest education, which requires a high school diploma, followed by social and healthcare assistants, social and healthcare helpers and nursing home assistants, and healthcare helper. Nursing home staff are unskilled workers. 1 = bad, 2 = less bad, 3 = good, 4 = very good, 5 = excellent. Shown are means and standard errors. MRSA was found among staff members. Our results thereby fall within the lower end of European studies which reported MRSA prevalence among staff ranging Fig. 2 Self-reported knowledge of methicillin-resistant S. aureus from 1.6% to 7.5% during non-outbreak times (Baldwin (MRSA). Shown are a) whether respondents had heard of MRSA, et al., 2009; Monaco et al., 2009; Peters et al., 2017), b) how they assess their knowledge, and c) how their average self- whereas levels outside Europe has been reported to range assessed knowledge differs among job groups. Nurses have the from 4%–90% (WHO, 2014). The low number found here longest education, which requires a high school diploma, followed is positive, since there may typically be a large risk of by social and healthcare assistants, social and healthcare helpers exposure to staff members in nursing homes, where MRSA and nursing home assistants, and healthcare helper. Nursing home staff are unskilled workers. 1 = bad, 2 = less bad, 3 = good, 4 = can be very prevalent among the residents (Garazi et al., very good, 5 = excellent. Shown are means and standard errors. 2009; Murphy et al., 2012), often exceeding levels in hospitals (Honda et al., 2010; Kurup et al., 2010). 8 Front. Environ. Sci. Eng. 2021, 15(3): 41 Furthermore, outbreaks among the residents can have with MRSA. This may highlight tasks that may lead to severe consequences for both staff and the residents (Koch higher exposure levels, however as MRSA was also et al., 2009). However, in S. aureus bacteraemia, MRSA detected in the background exposure, it shows that it is levels are generally low in Scandinavia< 1%–5% (Eur- crucial that proper precautions are taken in and when opean Centre for Disease Prevention and Control, 2019) leaving the residences of MRSA-colonised individuals. and therefore the level of MRSA among nursing home Furthermore, MSSA was found during cleaning of surfaces residents is probably much lower in Scandinavia than in and fomites and as background exposure in common areas, the rest of Europe. Future studies may examine whether indicating that with increasing antibiotic resistance, e.g. studying airborne bacterial DNA and using PCR would from abroad, there is the possibility that MRSA could be increase the detection limit of MRSA (e.g. Masclaux et al., observed in the places where MSSA was found. Lastly, the 2013), furthermore they may even distinguish between the MRSA spa types found in air, sedimented dust, and surface viable but not culturable fraction (White et al., 2020). In samples matched those of the colonised resident, thereby nursing homes in Europe, studies have found MRSA indicating that the MRSA isolates found comes from the colonisation levels of residents ranging from 0% to 23.3% resident. Similarly, Madsen et al. (2020) found a (Baldwin et al., 2009; Monaco et al., 2009; Andersson considerable overlap between the Staphylococcus species et al., 2012; Peters et al., 2017). Residents typically have a present in surface samples taken within the same high risk of contracting MRSA due to e.g. increased use of environment, and between bacterial species present in pharmaceuticals, chronic illness and use of devices such as surface samples, sedimented dust, and air samples within catheters (Garazi et al., 2009; Wibbenmeyer et al., 2010; the same environment Murphy et al., 2012; Peters et al., 2017). However, as the Generally, healthcare personnel in the nursing homes population of seniors is expected to grow in the coming reported to have good knowledge of MRSA and felt safe years, it is important to continue to avoid spread to working with residents who are colonised. However, our healthcare workers. This is especially important as care findings also show a small portion of staff members who workers can act as vectors for the transmission of MRSA to could benefit from further information on the topic, in other residents, both as carriers (Albrich and Harbarth, particular from certain job groups. The jobs groups which 2008) or through contaminated clothes (Morgan et al., generally reported lower knowledge was those of typically 2012; Roghmann et al., 2015). It is therefore vital that shorter educational background, and reported knowledge proper hygiene practices are met, not just for the staff about MRSA might therefore be linked to the level of members but also for the residents. education of staff. In addition, approximately one in three Staff members were exposed to MRSA during work in staff members at nursing homes report that they are the rooms of the residents colonised with MRSA in two of worried of contracting MRSA and one in two are worried the five nursing homes, both air samples, sedimented dust, about bringing it home to family and acquaintances and to and surface samples. Most studies of nursing homes have spread it to other residents. Similarly, in a study in Oslo, Norway, Thorstad et al. (2011) reported that half of the determined the exposure to MRSA through screenings of staff and residents (e.g. Baldwin et al., 2009; Andersson nursing home staff asked was concerned about becoming et al., 2012), or looked at bioaerosol exposure in hospital or infected with MRSA and the consequences this would indoor settings (Wilson et al., 2004; Li et al., 2015), but no have for their own social life, family, economy, and work studies have to our knowledge examined the bioaerosol restriction. This therefore further shows that continued exposure to MRSA in nursing homes, where unlike in education and awareness of MRSA is important among hospitals, MRSA-colonised residents are not isolated. nursing home staff members. Similar studies have however been done in residential Most respondents reported that they have good knowl- homes where authors have detected MRSA indoors edge on infection hygiene, however, less than half had read (Madsen et al., 2018) and found higher proportions of the Danish Health Authority’s guide to the prevention of antibiotic resistant S. aureus indoors than outdoors spread of MRSA (The Danish Health Authority, 2016). In (Gandara et al., 2006). MRSA can survive on surfaces comparison, an audit of healthcare workers in the UK and the main mode of spread is typically person-to-person showed that 67% of respondents had read the UK MRSA contact and contact with contaminated objects and apparel policy, though this differed among healthcare groups (Neely and Maley, 2000; Calfee et al., 2003; Mitchell et al., (Trigg et al., 2008). However, staff may get the proper 2015; Roghmann et al., 2015), however our findings information elsewhere, for example, as respondents confirm that MRSA can spread via inhaled particles in the reported here, e.g. from education, colleagues, hygiene air (Kozajda et al., 2019). This is particularly important, as nurses, and leaders. Based on the questionnaire it also many respondents in the questionnaire did not know that appears that infection hygiene guidelines are followed MRSA could be found in the air. well, and most also state that they always or almost always Staff members were exposed to MRSA in the air during follow the infection hygiene guidelines and that their personal care tasks, cleaning of floors, and as general workplace does. However, improvements could be made in background exposure in the rooms of residents colonised the use and availability of protective eyewear and Pil Uthaug Rasmussen et al. MRSA in nursing homes 9 Electronic Supplementary Material Supplementary material is available facemasks when there is risks of splashes or sprays of in the online version of this article at https://doi.org/10.1007/s11783-020- bodily fluids and that cleaning supplies (e.g., vacuum 1333-y and is accessible for authorized users. cleaners) are not used both in the residence of MRSA colonised individuals and elsewhere in the nursing home. Open Access This article is licensed under a Creative Commons Andersson et al. (2012) similarly found that personnel at Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give nursing homes in Stockholm, Sweden, reported good appropriate credit to the original author(s) and the source, provide a link to the knowledge on infection hygiene practices, but when Creative Commons licence, and indicate if changes were made. The images observed by researchers it was found that there were or other third party material in this article are included in the article’s Creative occasional shortcomings in the adherence to the guide- Commons licence, unless indicated otherwise in a credit line to the material. lines. Of course, there may be factors that makes full If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted compliance with infection hygiene guidelines hard. For use, you will need to obtain permission directly from the copyright holder. example, respondents point out a lack of cleaning To view a copy of this licence, visit http://creativecommons.org/licenses/by/ personnel, lack of knowledge of infection hygiene, lack 4.0/. of knowledge of MRSA, poor contact with residents with MRSA due to dementia or mental health, and economic challenges regarding increased care for resident with References MRSA as factors contributing to why hygiene guidelines are not always followed. Albrich W C, Harbarth S (2008). Health-care workers: Source, vector, or victim of MRSA? Lancet. Infectious Diseases, 8(5): 289–301 Andersson H, Lindholm C, Iversen A, Giske C G, Örtqvist Å, Kalin M, 5 Concluding remarks Fossum B (2012). Prevalence of antibiotic-resistant bacteria in residents of nursing homes in a Swedish municipality: Healthcare Our study confirms that MRSA can be found in the air, in staff knowledge of and adherence to principles of basic infection sedimented dust and on surfaces, where it may work as an prevention. Scandinavian Journal of Infectious Diseases, 44(9): 641– important transmission route. Furthermore, our study indicates that the prevalence of MRSA is low during Baldwin N S, Gilpin D F, Hughes C M, Kearney M P, Gardiner D A, non-outbreak times among nursing home staff in the Cardwell C, Tunney M M (2009). Prevalence of methicillin-resistant Capital Region of Denmark, and that exposure to MRSA is Staphylococcus aureus colonization in residents and staff in nursing low but confined to the residences of residents with MRSA homes in Northern Ireland. Journal of the American Geriatrics colonisation. While infection hygiene practices seem to be Society, 57(4): 620–626 followed well, our results also show room for improve- Bartels M D, Larner-Svensson H, Meiniche H, Kristoffersen K, ment. Key areas to highlight based on the questionnaire is Schønning K, Nielsen J B, Rohde S M, Christensen L B, Skibsted the lack of knowledge of aerial spread of MRSA, that A W, Jarløv J O, Johansen H K, Andersen L P, Petersen I S, Crook D MSSA and MRSA give the same infections, the lack of W, Bowden R, Boye K, Worning P, Westh H (2015). Monitoring easy access and use of protective face and eyewear during meticillin resistant Staphylococcus aureus and its spread in work with risk of splashes, and that a large portion of staff Copenhagen, Denmark, 2013, through routine whole genome members worry about contracting MRSA and spreading it sequencing. Eurosurveillance, 20(17): 21112 to family and residents. As knowledge on both MRSA and Bates D, Maechler M, Bolker B, Walker S (2014). LME4: linear Mixed– infection hygiene differs among job groups, it is important Effects Models Using Eigen and S4 that each nursing home continue to educate their personnel Böcher S, Middendorf B, Westh H, Mellmann A, Becker K, Skov R, on multidrug resistant organisms and proper infection Friedrich A W (2010). Semi-selective broth improves screening for control, including staff members of shorter educational methicillin-resistant Staphylococcus aureus. Journal of Antimicrobial background and perhaps those who are not directly Chemotherapy, 65(4): 717–720 working with care tasks. This may reduce the level of Bradley S F (1999). Methicillin-resistant Staphylococcus aureus. worry about MRSA that staff reported. Maintaining proper American Journal of Medicine, 106(5 Supplement 1): 2–10 hygiene practices and adhering to guidelines is especially Calfee D P, Durbin L J, Germanson T P, Toney D M, Smith E B, Farr B important, because failure to do so may cause outbreaks M (2003). Spread of methicillin-resistant Staphylococcus aureus among the residents, which could have severe conse- (MRSA) among household contacts of individuals with nosocomially quences for both staff and the residents. acquired MRSA. Infection Control and Hospital Epidemiology, 24 Acknowledgements We would like to thank all the participants in the (6): 422–426 study. We would also like to thank Prof. Dr. Monika Raulf for EDC supply. Calfee D P, Salgado C D, Milstone A M, Harris A D, Kuhar D T, Moody We acknowledge Margit W. Frederiksen, the National Research Institute of J, Aureden K, Huang S S, Maragakis L L, Yokoe D S (2014). the Working Environment, Denmark, for excellent technical assistance. This Strategies to prevent methicillin-resistant Staphylococcus aureus work was supported by grant 16-B-0239 from Helsefonden and by the Danish transmission and infection in acute care hospitals: 2014 Update. Government through a grant to the FOR-SOSU program (SATS 2004) at the National Research Centre for the Working Environment, Denmark. Infection Control and Hospital Epidemiology, 35(7): 772–796 10 Front. Environ. Sci. Eng. 2021, 15(3): 41 CDC (2013). Antibiotic Resistance Threats in the United States. and MSSA), total bacteria, and endotoxins in pig farms. Annals of Washington, DC: Centers for Disease Control Occupational Hygiene, 57(5): 550–557 DANMAP (2018). Use of antimicrobial agents and occurrence of Mitchell A, Spencer M, Edmiston C Jr (2015). Role of healthcare apparel antimicrobial resistance in bacteria from food animals, food and and other healthcare textiles in the transmission of pathogens: A humans in Denmark. Copenhagen: DANMAP review of the literature. Journal of Hospital Infection, 90(4): 285– Danmarks Statistik (2020). FOLK1A. Copenhagen: Danmarks Statistik 292 European Centre for Disease Prevention and Control (2019). 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Concentration of airborne Staphylococcus aureus (MRSA Hygiene and Environmental Health, 230: 113608 Pil Uthaug Rasmussen et al. MRSA in nursing homes 11 WHO (2014). Antimicrobial Resistance: Global Report on Surveillance. Care & Research; Official Publication of the American Burn Geneva: World Health Organization Association, 31(2): 269–279 Wibbenmeyer L, Williams I, Ward M, Xiao X, Light T, Latenser B, Wilson R D, Huang S J, Mclean A S (2004). The correlation between Lewis R, Kealey G P, Herwaldt L (2010). Risk factors for acquiring airborne methicillin-resistant Staphylococcus aureus with the vancomycin-resistant Enterococcus and methicillin-resistant Staphy- presence of MRSA colonized patients in a general intensive care lococcus aureus on a burn surgery step-down unit. Journal of Burn unit. Anaesthesia and Intensive Care, 32(2): 202–209 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png "Frontiers of Environmental Science & Engineering" Springer Journals

Occupational risk of exposure to methicillin-resistant Staphylococcus aureus (MRSA) and the quality of infection hygiene in nursing homes

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Front. Environ. Sci. Eng. 2021, 15(3): 41 https://doi.org/10.1007/s11783-020-1333-y RESEARCH ARTICLE Occupational risk of exposure to methicillin-resistant Staphylococcus aureus (MRSA) and the quality of infection hygiene in nursing homes 1 1 2 2 Pil Uthaug Rasmussen (✉) , Katrine Uhrbrand , Mette Damkjær Bartels , Helle Neustrup , Dorina Gabriela 1,3 1,4 1 Karottki , Ute Bültmann , Anne Mette Madsen 1 National Research Centre for the Working Environment, Lersø Parkallé 105, 2100 Copenhagen Ø, Denmark 2 Department of Clinical Microbiology, Hvidovre Hospital, Kettegård Allé 30, 2650 Hvidovre, Denmark 3 The Danish Working Environment Authority, Landskronagade 33, 2100 Copenhagen, Denmark 4 University Medical Center Groningen, Department of Health Sciences, Community & Occupational Medicine, University of Groningen, 9700 Groningen, The Netherlands HIGH LIGHTS GRAPHIC A BSTRA C T � Staff members were not colonised with MRSA. � But staff were exposed to MRSA from air, sedimented dust and surfaces. � MRSA was found in the rooms of MRSA- colonised residents but not in common areas. � Staff worry about MRSA and spreading it to other residents, family, and acquaintances. � The use of protective eyewear and facemasks could be improved. AR TICL E I N F O ABSTRA CT Article history: Methicillin-resistant Staphylococcus aureus (MRSA) is an increasing health concern across the globe and is often prevalent at long-term care facilities, such as nursing homes. However, we know little of Received 6 July 2020 whether nursing home staff is exposed to MRSA via air and surfaces. We investigated whether staff Revised 4 September 2020 members at nursing homes are colonised with and exposed to culturable MRSA, and assessed staff Accepted 7 October 2020 members’ self-reported knowledge of MRSA and compliance with infection hygiene guidelines. Five Available online 13 November 2020 nursing homes with MRSA positive residents were visited in Copenhagen, Denmark. Personal bioaerosol exposure samples and environmental samples from surfaces, sedimented dust and bioaerosols were examined for MRSA and methicillin-susceptible S. aureus (MSSA) to determine Keywords: occupational exposure. Swabs were taken from staffs’ nose, throat, and hands to determine whether they were colonised with MRSA. An online questionnaire about MRSA and infection control was Antibiotic resistance distributed. No staff members were colonised with MRSA, but MRSAwas detected in the rooms of the Airborne MRSA colonised residents in two out of the five nursing homes. MRSA was observed in air (n = 4 out of 42, Bioaerosols 3 3 2 ranging from 2.9–7.9 CFU/m ), sedimented dust (n = 1 out of 58, 1.1  10 CFU/m /d), and on Healthcare-associated infections surfaces (n = 9 out of 113, 0.04–70.8 CFU/m ). The questionnaire revealed that half of the staff Healthcare worker members worry about spreading MRSA to others. Identified aspects for improvement were improved Occupational health availability and use of protective equipment, not transferring cleaning supplies (e.g., vacuum cleaners) between residents’ rooms and to reduce worry of MRSA, e.g., through education. © The Author(s) 2020. This article is published with open access at link.springer.com and journal.hep. com.cn ✉ Corresponding author E-mail: pur@nfa.dk Special Issue—Bioaerosol, Environment and Health (Responsible Editors: Can Wang, Jungho Hwang, Jingkun Jiang & Maosheng Yao) 2 Front. Environ. Sci. Eng. 2021, 15(3): 41 members, or if staff members are colonised with MRSA 1 Introduction they can act as vectors to other residents or colleagues (Albrich and Harbarth, 2008).We therefore need i) more More than 40000 seniors (i.e. over 65 years) are currently information on the transfer of MRSA via air and surfaces residing in nursing homes in Denmark (Sundheds- Og within nursing home settings and the risks it poses for the ldreministeriet, 2016). This number is expected to increase staff, and ii) to understand the staff’s experience with in the coming years (Danmarks Statistik, 2020). In MRSA and compliance with infection hygiene guidelines. Denmark, half of the residents have one or more chronic To answer these questions five nursing homes, which had disease and over two thirds have dementia (Sundheds- Og residents colonised with MRSA were visited twice in the ldreministeriet, 2016). The residents also have an Capital Region of Denmark. Staff members were screened increased use of pharmaceuticals, are more in contact for MRSA, and bioaerosol, sedimented dust, and surface with doctors, and have more admissions to the hospital samples were taken. Furthermore, a questionnaire about than others of the same age who do not live in nursing MRSA and hygiene practices was sent to nursing home homes (Sundheds- Og ldreministeriet, 2016). These staff members in four of the nursing homes. The study factors are contributing to the typically high prevalence of aimed at answering whether MRSA is present on the hands multidrug-resistant microorganisms and MRSA in nursing and in the airways of nursing home staff, whether nursing homes (Bradley, 1999; Stone et al., 2008; Garazi et al., home staff is exposed to MRSA or MSSA during their 2009). We therefore need more information on the risk of work in both the colonised residents’ rooms and in occupational exposure to multidrug-resistant microorgan- common areas, and what the level of knowledge and isms for healthcare workers. experience of staff members to MRSA and infection Multidrug-resistant microorganisms, such as methicil- hygiene is. lin-resistant Staphylococcus aureus (MRSA), a bacterium resistant to many of the antibiotics typically used for treatment, is a worldwide concern (CDC, 2013; WHO, 2 Materials and methods 2014; DANMAP, 2018). MRSA accounts for more than half of S. aureus infections worldwide (WHO, 2014), but 2.1 Sampling location and participants in Denmark, the incidence level is low, with almost 4000 new cases in 2018 constituting only 1.6% of S. aureus Sampling was carried out from October 2017 to June 2018 bacteraemia cases (DANMAP, 2018). To avoid spread, at five nursing homes (A-E) in the Capital Region of adequate precautions have to be taken when healthcare Denmark with residents known to be MRSA-colonised. personnel are interacting with MRSA-infected or – The nursing homes were selected because they had at least colonised individuals (Calfee et al., 2014). In hospitals, one MRSA positive resident who was monitored at the this includes isolation of patients in their rooms (Calfee MRSA Knowledge Center at Hvidovre Hospital. Each et al., 2014). In Danish nursing homes, isolation of nursing home was visited on two separate occasions with residents with MRSA is not allowed unless they have a 14 days apart and 52 staff members in different job respiratory infection. In addition, rooms are rented to the functions participated in the study. A total of 79 personal residents who have some autonomy in their own rooms, exposure assessments were conducted as some staff while healthcare and cleaning personnel assist with members participated on both of the two sampling days. personal care and cleaning. Residents are fully integrated Four to eleven personal assessments were done per into everyday activities at the nursing home and in sampling day, and of the 79 assessments conducted, 8 common areas, and this may facilitate MRSA transmission (10%) were on nurses, 37 (47%) were on social and and increase the exposure of staff members in nursing healthcare assistants, 15 (19%)wereonsocialand homes when interacting directly and indirectly with healthcare helpers, 7 (9%) were on cleaning assistants, individuals colonised with MRSA. Nevertheless, little is and 12 (15%) were on staff with other job titles. known about the degree to which nursing home staff Participation was voluntary and all staff members and members are exposed to, colonised with, or infected with residents colonised with MRSA signed a consent form methicillin-susceptible S. aureus (MSSA) and MRSA, before entering the project. The resident had to give both especially in regards to airborne MRSA, which for many oral and written consent to have MRSA samples taken may be an overlooked transmission route (Kozajda et al., from the environment of their room. Ethical approval was 2019). According to the MRSA guidelines from the Danish applied for, but the National Committee on Health Health Authority, extended hygiene practices have to be Research Ethics decided an approval was not needed for met when taking care of the infected or colonised residents the types of samples taken (swabs and bioaerosol and when cleaning their room (The Danish Health measurements), as only microorganisms but not biological Authority, 2016). If adequate hygiene practices are not material was taken from the participants. met, there may be a higher risk of exposure to staff Pil Uthaug Rasmussen et al. MRSA in nursing homes 3 2.2 MRSA screening of staff sampled for 20 min at a flow rate of 3.5 L/min. In addition, stationary air sampling was performed by collecting Staff members were screened for MRSA in the nose, throat bacteria directly on SA agar using a six-stage Andersen and on their hands at the beginning and end of the working Cascade Impactor (ACI; N6, Thermo Fisher Scientific Inc. day. Sampling was done using the eSwab transport system Waltham, MA, USA) with a flow rate of 28.3 L/min (eSwab; Copan, Brescia, Italy) which consists of a flocked measuring for an average of 10 minutes and at a height of 1 nylon swab and 1 ml transport medium. Nasal samples m. ACI samples were stored in a cool box and incubated were taken from the anterior nares by rotating the same directly at 37°C for 48 h upon return to the laboratory. swabs in each nostril. Throat samples were obtained by Electrostatic dust cloths (EDCs; ZEEMAN, Alphen, swabbing the palatopharyngeal arch and tonsils on both Holland, surface exposure area of 0.0209 m (19 cm  11 sides. Hand samples were collected by rotating the eSwabs cm)) were used for long-term passive sampling of axially and laterally in a zigzag motion over the entire sedimented dust. On each sampling visit, EDCs were surface of each palm, using the same swabs on both right placed on an open surface and dust allowed to settle for 7 d. and left hand. After sampling, all swabs were transferred to EDCs were placed in the residences of the MRSA- their container, stored cold (4°C), and processed within 24 colonised individuals, common areas, corridors in com- hours of sampling. Hand samples were vortexed for 2 min, mon areas, staff changing rooms, staff offices, and laundry plated in serial-dilutions on chromogenic SaSelect agar rooms at a height ranging from 0.7–1.8 m. In total, 11–12 (SA; Biorad, Solna, Sweden) and incubated at 37°C for 48 EDCs were placed per nursing home. hours. Eswabs from nose and throat samples were An outdoor stationary reference measurement was taken inoculated into MRSA enrichment broth (TSB containing at every sampling. Outdoor references were taken with a 2.5% NaCl, 3.5 mg/L cefoxitin, and 20 mg/L aztreonam; GSP placed at a height of 1.5 m. The average sampling (Böcher et al., 2010)) and incubated overnight at 35°C. Ten time of the reference measurements was 385 min. µl of broth was then inoculated onto a selective MRSA Temperature and relative humidity were measured inside plate (Brilliance MRSA 2 agar, Oxoid, Thermo Fisher and outside the nursing homes during sampling using Scientific) and an unselective 5% Danish Blood agar plate Tinytag Plus Data Loggers (Germini Data Loggers, United and incubated overnight. Colonies suggestive of S. aureus Kingdom; Table S1). were identified using matrix-assisted laser desorption- Bacteria from all GSP filters and EDC cloths were ionisation time-of-flight (MALDI-TOF) mass spectro- extracted in 5 and 20 mL of pyrogen-free water containing metry (MS) and their susceptibility to cefoxitin (30 µg) 0.85% NaCl and 0.05% Tween 80, respectively. Staphy- was determined. For isolates resistant to cefoxitin accord- lococci bacteria were enumerated by dilution plating and ing to EUCAST breakpoints, the presence of mecAor incubation on SA agar at 37°C for 48 h. mecC was confirmed by an in-house PCR. Environmental surface sampling of armrests, tables, door handles, light switches, and TV remotes was 2.3 Exposure to MRSA conducted in the MRSA individuals’ residences and in the common areas of the nursing homes (on average 10 To collect bacteria from the inhalation zone of the nursing swabs in total of each type, both in residences and common home staff, personal air samplers (Gesamtstaubprobe- rooms), and surface samples were furthermore taken from nahme sampler (GSP), CIS, BGI Inc., Waltham, MA, the bed rails of the resident colonised with MRSA (n = 10). USA) mounted with a 37 mm polycarbonate filter (PC, Sampling was done using eSwabs by rotating the swab pore size 1.0 µm, Main Manufacturing, Grand Blanc, axially and laterally in a zigzag motion over a surface area MI, USA) and a flow rate of 3.5 L/min were used. The of approximately 100 cm . Samples were stored and personal GSP samplers, connected to pumps worn in a processed as described for the hand swabs. backpack, were placed in the breathing zone of the participants. The GSP was chosen, as it samples inhalable 2.4 Identification and molecular characterization of MRSA particles (airflow 3.5 L/min), and as it has been described isolates to have a good sampling efficiency (Kenny et al., 1999). The personal air sampling was performed during an entire Presumptive S. aureus isolates were recognized based on working day while the nursing home staff performed morphological appearance on SA media. Identification was normal job tasks. The average personal air sampling period performed on all the presumptive S. aureus isolates from was 315 min. all samples using MALDI-TOF MS as described in (Feld To collect air samples during specific work tasks, e.g. et al., 2018). All S. aureus isolates from exposure samples while providing assistance to the resident colonised with were tested for methicillin resistance by sub cultivation on MRSA or during cleaning of their residence, stationary Brilliance MRSA 2agarfor 24 hat37°C. One short-term air sampling was used. For this, a GSP sampler presumptive MRSA isolate from each sample was selected with a PC filter was placed at a fixed height of 1.5 m and for molecular verification and were confirmed to be MRSA 4 Front. Environ. Sci. Eng. 2021, 15(3): 41 by an in-house multiplex PCR targeting the genes mecA, 2.6 Data and statistical analyses mecC, nuc and femA. MRSA isolates were then whole genome sequenced on an Illumina MiSeq and assembled Bacterial concentrations were calculated as geometric 3 3 mean (GM) concentration per m of air (CFU/m ) for as previously described (Bartels et al., 2015). cgMLST was GSP and ACI air samples, as GM concentration per m per performed using the Ridom SeqSphere software and the day (CFU/m /d) for EDC samples, as GM concentration isolates were compared to the whole genome sequenced 2 2 per cm (CFU/cm ) for surface samples, and GM isolates from the MRSA colonised patients from the concentration per hands (CFU/hands) for hand samples. specific nursing home in order to confirm whether the Limits of detection was on average: personal GSP = 8.2 environmental MRSA was identical to the isolate of the 3 3 CFU/m , GSP during tasks = 47.6 CFU/m , ACI during patient. 3 2 tasks = 2.9 CFU/m , EDC = 91.1 CFU/m /d, eSwabs were 0.04 CFU/cm for surfaces and 8.3 CFU/ hands for hand 2.5 Questionnaire swabs. A self-administered questionnaire was distributed among In order to investigate the impact of nursing home and the staff members of four nursing homes (A, B, C, E) job group on responses to the questionnaire, we ran linear covering approximately 100 questions on knowledge mixed effect models with nursing home, job and their regarding MRSA and infection hygiene. Due to time interaction as fixed effects. For questions where respon- constraints at the nursing home, staff members at nursing dents had to give a rating of e.g. their knowledge, the home D did not participate. The questionnaire inquired answers were given on a scale from 1–5, and otherwise about the participant’s background, knowledge of and answers were treated as categories. All analyses were experience with MRSA and infection hygiene, compliance conducted in R v.3.5.3 (R. Core Team, 2019), using with infection hygiene guidelines, and opinions on the packages lme4 v. 1.1–24 and car v. 3.0–3 (Fox and consequences of working with residents with MRSA. The Weisberg, 2011; Bates et al., 2014). questionnaire was sent to 161 nursing home staff members, and 74 respondents answered the questionnaire (46% 3 Results response rate). Both complete (n = 51) and partial (n = 23) completions were included in the analyses. Due to the 3.1 Exposure to MRSA length of the questionnaire, we only report key findings in the Results section, but a full description can be found in MALDI-TOF identification was attempted on bacterial the Supplementary Information (Results S1, Tables S2– isolates from the stationary ACI air samples, stationary and S6). Table 1 Staphylococcus aureus and methicillin-resistant S. aureus (MRSA) found during screening of staff members and the exposure to MRSA in air, surface and sedimented dust samples. Percentages calculated based on the total number of samples S. aureus positive samples MRSA positive samples Total number Sample group of samples % n Concentration % n Concentration MRSA screening of staff –– 158 00 Nasal swab –– 156 00 Throat swab 158 10.8 17 10–150 CFU/hand 0 0 Hand swab 472 3.6% 17 0 0 Total of all screening samples Exposure to MRSA 79 15.2 12 7.3–201.9 CFU/m 00 Personal GSP air sample 46 6.5 3 285.7–1857.1 CFU/m 00 Stationary GSP air sample 3 3 42 21.4 9 2.9–173.1 CFU/m 9.5 4 2.9–7.9 CFU/m 6-stage ACI stationary air sample 2 3 2 58 8.6 5 91.1–1093.6 CFU/m /d 1.7 1 1.1  10 CFU/m /d EDC sedimented dust sample 2 2 113 23.6 26 0.04–70.8 CFU/cm 8.2 9 0.04–70.8 CFU/cm Surface sample Total of all exposure samples 338 16.3% 55 4.1% Stationary GSP outdoor air reference 10 0 0 0 Staff members were screened for MRSA at the start and end of the working day. Incidence of S. aureus was not determined for nasal and throat samples. ACI = stationary six-stage Andersen Cascade Impactor, GSP = stationary Gesamtstaubprobenahme sampler, EDC = electrostatic dust cloth. Each 6-stage ACI stationary air sample was grown on six chromogenic SaSelect agar plates, but here all six plates are presented as one sample. Pil Uthaug Rasmussen et al. MRSA in nursing homes 5 personal GSP air samples, outdoor reference air samples, whereas MSSA was detected in all sample types and in surfaces samples, and hand swabs. In total, 423 S. aureus both the common areas and in the residences. MRSA was isolates were identified, and these were found in 72 out of found during specific work tasks: during personal care the 496 samples examined for S. aureus (Table 1). Of the S. tasks, cleaning of floors, and in the background air aureus isolates, 25.3% (107 isolates) were presumed to be measurements (Table 2). MRSA was observed in particles methicillin resistant. These MRSA isolates were found in a in the size range of 4.7 µm and above. total of 14 samples, consisting of 4 stationary ACI air MSSA was found on surfaces both in common areas and samples, 1 EDC sample, and 9 surface samples (Table 1). the colonised residents’ room (Table 3). However, MRSA MRSAwas not detected in nose, throat or hand swabs from was only detected in the room of the resident colonised the staff members (neither at the beginning nor at the with MRSA on armrests, bed rails, TV-remotes, and on the end of the working day), in any of the stationary or door handles (Table 3). personal GSP air samples, nor in references air samples (Table 1). 3.2 Knowledge of MRSA and infection hygiene Overall, MRSA was detected in the colonised-residents’ room but not in common areas, and while MSSA was The majority of respondents (97% and 77%, respectively) present at all nursing homes, MRSA was only detected in had heard of and reported their knowledge about MRSA as two of the five nursing homes. Whole genome sequencing good, very good or excellent (Figs. 2(a)–2(b)), however, showed that the MRSA spa types (t) and multilocus knowledge of MRSA differed among job groups (F = 6,42 sequence types (ST) (t3841/ST672 and t223/ST22) found 3.67, P = 0.008; Fig. 2(c)). Most respondents (83%) at each nursing home matched that of the infected resident similarly rated their knowledge of infection hygiene as at that home (Fig. 1). good, very good or excellent (Fig. 3(a)), though this again differed among job groups (F = 3.67, P = 0.029; Fig. 3 6,49 (b)). Thirty-eight percent of respondents had heard of but not read the ‘Guideline for prevention of spread of MRSA’ from the Danish Health Authority, and 21% had not heard of it. Ninety percent reported that they always or mostly always followed the infection hygiene guidelines, but this differed among job groups and nursing homes (a significant interaction effect; F = 2.14, P = 0.039). 12,36 Eighty-one percent reported that their workplace as a whole always or almost always followed the guidelines. The majority of the respondents reported easy access to personal protective equipment such as gloves and protective clothing. However, protective eyewear (incl. visors) and facemasks (surgical masks and respirators) seemed to be less easily available. Around 40% and 10% of the respondents reported that they did not have easy access to protective eyewear and facemasks, respectively. The level of easy access differed among nursing homes (protective eyewear: F = 2.27, P = 0.097; facemasks: 3,36 F =7.94, P< 0.001). For staff with care tasks, 3,36 facemasks was used most of the time when there was a risk of splashes and sprays of bodily fluids, however a large group (19%) stated that they never use it. Similarly, 50% said they never use protective eyewear in similar situations. Cleaning supplies (e.g., vacuums) sometimes gets transferred from the MRSA residents’ room to other Fig. 1 Whole genome clustering of methicillin-resistant S. places of the nursing home (15% state it always happens aureus (MRSA) isolates at the two nursing homes (a) and and 8% that it sometimes happens). Respondents reported (b) were MRSA was detected. MRSA isolates starting with M is that they are a lot or very much (30%) worried about from the colonised residents, while isolates starting with WGS are contracting MRSA, a lot or very much (49%) worried from surface and air samples collected at the nursing home. about bringing MRSA from work to family and acquain- tances, and a lot and very much (45%) worried about being Air and sedimented dust samples showed that the the cause of transfer of MRSA to other residents in the nursing home staff members were exposed to MRSA in the nursing home. Whether contracting MRSA would have a air of the MRSA-colonised resident’s room (Table 1–2), negative influence on respondents’ social lives, 52% 6 Front. Environ. Sci. Eng. 2021, 15(3): 41 Table 2 Potential exposure to Staphylococcus aureus and methicillin-resistant S. aureus (MRSA) in air samples during specific work tasks conducted in the room of the MRSA-colonised resident. Shown are samples positive for S. aureus and MRSA S. aureus positive samples MRSA positive samples Total number of Work task GM Range GM Range samples n n 3 3 3 3 (CFU/m ) (CFU/m ) (CFU/m ) (CFU/m ) ACI Personal care 6 21.1 8.9–56.5 2 7.9 – 1 Cleaning of surfaces & fomites 9 134.3 – 1- – 0 Cleaning of floors 6 4.8 3.5–7.9 3 5.6 3.9–7.9 2 –– –– Bed making 2 0 0 –– –– Nursing tasks 2 0 0 Background; MRSA residence 8 22.6 2.9–173.1 2 2.9 1 Background; Common area 9 3.5 – 1 – 0 GSP – –– Personal care 9 285.7 1 0 – –– 0 Cleaning of surfaces & fomites 5 – 0 – –– 0 Cleaning of surfaces, fomites & floor 4 1857.1 1 –– –– 0 Cleaning of floors 4 0 –– –– 0 Bed making 2 0 –– –– 0 Nursing tasks 2 0 –– –– Other (marking of clothes) 1 - – –– 0 Background; MRSA residence 8 571.4 1 –– –– 0 Background; common area 11 0 –– –– Outdoor GSP reference 10 0 0 Geometric means (GM), ranges, and number (n) of positive S. aureus and MRSA samples. A hyphen is listed where no positive samples were observed or for ranges when only one positive sample was found. ACI = stationary six-stage Andersen Cascade Impactor, GSP = stationary Gesamtstaubprobenahme sampler. Values from ACI samples are sums of all the six stages. Table 3 Surface samples found positive for Staphylococcus aureus and methicillin-resistant S. aureus (MRSA) in the residences of the MRSA- colonised individuals and in the common areas of the nursing homes Residence of MRSA-colonised individual Common area S. aureus MRSA positive S. aureus MRSA positive positive samples samples positive samples samples Sampling point Number of Number of GM GM GM GM samples samples % n (CFU % n (CFU % n (CFU/ % n (CFU/ 2 2 2 2 /cm ) “/cm ) cm ) cm ) Armrest 10 30 3 0.53 30 3 0.33 10 30 3 0.19 0 0 Table 10 10 1 1 0 0 – 10 30 3 0.37 0 0 Door handle 11 18 2 8.28 9 1 5.33 12 42 5 0.88 0 0 – – Light switch 10 10 1 0.24 0 0 – 10 0 0 00 – – TV remote 10 30 3 0.49 20 2 0.19 10 0 0 00 –– – – – – Bed rail 10 40 4 3.63 30 3 3.07 0 As beds are only located in residents’ rooms, no bed rail samples were taken from common areas. answered that they agreed or completely agreed, however 4 Discussion this depended on both nursing home and job group (F = 3,29 3.05, P = 0.044; F = 2.50, P = 0.045), where 6,42 Our study showed that staff members working in nursing respondents from two of the nursing home mainly reported homes in The Capital Region of Denmark were not they neither agreed nor disagreed, but respondents from the colonised with culturable MRSA, similar to findings in two other nursing homes were mainly more worried. Stockholm, Sweden (Andersson et al., 2012) where no Pil Uthaug Rasmussen et al. MRSA in nursing homes 7 Fig. 3 Self-reported knowledge of infection hygiene. Shown are a) how respondents assess their knowledge, and b) how their average self-assessed knowledge differs among job groups. Nurses have the longest education, which requires a high school diploma, followed by social and healthcare assistants, social and healthcare helpers and nursing home assistants, and healthcare helper. Nursing home staff are unskilled workers. 1 = bad, 2 = less bad, 3 = good, 4 = very good, 5 = excellent. Shown are means and standard errors. MRSA was found among staff members. Our results thereby fall within the lower end of European studies which reported MRSA prevalence among staff ranging Fig. 2 Self-reported knowledge of methicillin-resistant S. aureus from 1.6% to 7.5% during non-outbreak times (Baldwin (MRSA). Shown are a) whether respondents had heard of MRSA, et al., 2009; Monaco et al., 2009; Peters et al., 2017), b) how they assess their knowledge, and c) how their average self- whereas levels outside Europe has been reported to range assessed knowledge differs among job groups. Nurses have the from 4%–90% (WHO, 2014). The low number found here longest education, which requires a high school diploma, followed is positive, since there may typically be a large risk of by social and healthcare assistants, social and healthcare helpers exposure to staff members in nursing homes, where MRSA and nursing home assistants, and healthcare helper. Nursing home staff are unskilled workers. 1 = bad, 2 = less bad, 3 = good, 4 = can be very prevalent among the residents (Garazi et al., very good, 5 = excellent. Shown are means and standard errors. 2009; Murphy et al., 2012), often exceeding levels in hospitals (Honda et al., 2010; Kurup et al., 2010). 8 Front. Environ. Sci. Eng. 2021, 15(3): 41 Furthermore, outbreaks among the residents can have with MRSA. This may highlight tasks that may lead to severe consequences for both staff and the residents (Koch higher exposure levels, however as MRSA was also et al., 2009). However, in S. aureus bacteraemia, MRSA detected in the background exposure, it shows that it is levels are generally low in Scandinavia< 1%–5% (Eur- crucial that proper precautions are taken in and when opean Centre for Disease Prevention and Control, 2019) leaving the residences of MRSA-colonised individuals. and therefore the level of MRSA among nursing home Furthermore, MSSA was found during cleaning of surfaces residents is probably much lower in Scandinavia than in and fomites and as background exposure in common areas, the rest of Europe. Future studies may examine whether indicating that with increasing antibiotic resistance, e.g. studying airborne bacterial DNA and using PCR would from abroad, there is the possibility that MRSA could be increase the detection limit of MRSA (e.g. Masclaux et al., observed in the places where MSSA was found. Lastly, the 2013), furthermore they may even distinguish between the MRSA spa types found in air, sedimented dust, and surface viable but not culturable fraction (White et al., 2020). In samples matched those of the colonised resident, thereby nursing homes in Europe, studies have found MRSA indicating that the MRSA isolates found comes from the colonisation levels of residents ranging from 0% to 23.3% resident. Similarly, Madsen et al. (2020) found a (Baldwin et al., 2009; Monaco et al., 2009; Andersson considerable overlap between the Staphylococcus species et al., 2012; Peters et al., 2017). Residents typically have a present in surface samples taken within the same high risk of contracting MRSA due to e.g. increased use of environment, and between bacterial species present in pharmaceuticals, chronic illness and use of devices such as surface samples, sedimented dust, and air samples within catheters (Garazi et al., 2009; Wibbenmeyer et al., 2010; the same environment Murphy et al., 2012; Peters et al., 2017). However, as the Generally, healthcare personnel in the nursing homes population of seniors is expected to grow in the coming reported to have good knowledge of MRSA and felt safe years, it is important to continue to avoid spread to working with residents who are colonised. However, our healthcare workers. This is especially important as care findings also show a small portion of staff members who workers can act as vectors for the transmission of MRSA to could benefit from further information on the topic, in other residents, both as carriers (Albrich and Harbarth, particular from certain job groups. The jobs groups which 2008) or through contaminated clothes (Morgan et al., generally reported lower knowledge was those of typically 2012; Roghmann et al., 2015). It is therefore vital that shorter educational background, and reported knowledge proper hygiene practices are met, not just for the staff about MRSA might therefore be linked to the level of members but also for the residents. education of staff. In addition, approximately one in three Staff members were exposed to MRSA during work in staff members at nursing homes report that they are the rooms of the residents colonised with MRSA in two of worried of contracting MRSA and one in two are worried the five nursing homes, both air samples, sedimented dust, about bringing it home to family and acquaintances and to and surface samples. Most studies of nursing homes have spread it to other residents. Similarly, in a study in Oslo, Norway, Thorstad et al. (2011) reported that half of the determined the exposure to MRSA through screenings of staff and residents (e.g. Baldwin et al., 2009; Andersson nursing home staff asked was concerned about becoming et al., 2012), or looked at bioaerosol exposure in hospital or infected with MRSA and the consequences this would indoor settings (Wilson et al., 2004; Li et al., 2015), but no have for their own social life, family, economy, and work studies have to our knowledge examined the bioaerosol restriction. This therefore further shows that continued exposure to MRSA in nursing homes, where unlike in education and awareness of MRSA is important among hospitals, MRSA-colonised residents are not isolated. nursing home staff members. Similar studies have however been done in residential Most respondents reported that they have good knowl- homes where authors have detected MRSA indoors edge on infection hygiene, however, less than half had read (Madsen et al., 2018) and found higher proportions of the Danish Health Authority’s guide to the prevention of antibiotic resistant S. aureus indoors than outdoors spread of MRSA (The Danish Health Authority, 2016). In (Gandara et al., 2006). MRSA can survive on surfaces comparison, an audit of healthcare workers in the UK and the main mode of spread is typically person-to-person showed that 67% of respondents had read the UK MRSA contact and contact with contaminated objects and apparel policy, though this differed among healthcare groups (Neely and Maley, 2000; Calfee et al., 2003; Mitchell et al., (Trigg et al., 2008). However, staff may get the proper 2015; Roghmann et al., 2015), however our findings information elsewhere, for example, as respondents confirm that MRSA can spread via inhaled particles in the reported here, e.g. from education, colleagues, hygiene air (Kozajda et al., 2019). This is particularly important, as nurses, and leaders. Based on the questionnaire it also many respondents in the questionnaire did not know that appears that infection hygiene guidelines are followed MRSA could be found in the air. well, and most also state that they always or almost always Staff members were exposed to MRSA in the air during follow the infection hygiene guidelines and that their personal care tasks, cleaning of floors, and as general workplace does. However, improvements could be made in background exposure in the rooms of residents colonised the use and availability of protective eyewear and Pil Uthaug Rasmussen et al. MRSA in nursing homes 9 Electronic Supplementary Material Supplementary material is available facemasks when there is risks of splashes or sprays of in the online version of this article at https://doi.org/10.1007/s11783-020- bodily fluids and that cleaning supplies (e.g., vacuum 1333-y and is accessible for authorized users. cleaners) are not used both in the residence of MRSA colonised individuals and elsewhere in the nursing home. Open Access This article is licensed under a Creative Commons Andersson et al. (2012) similarly found that personnel at Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give nursing homes in Stockholm, Sweden, reported good appropriate credit to the original author(s) and the source, provide a link to the knowledge on infection hygiene practices, but when Creative Commons licence, and indicate if changes were made. The images observed by researchers it was found that there were or other third party material in this article are included in the article’s Creative occasional shortcomings in the adherence to the guide- Commons licence, unless indicated otherwise in a credit line to the material. lines. Of course, there may be factors that makes full If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted compliance with infection hygiene guidelines hard. For use, you will need to obtain permission directly from the copyright holder. example, respondents point out a lack of cleaning To view a copy of this licence, visit http://creativecommons.org/licenses/by/ personnel, lack of knowledge of infection hygiene, lack 4.0/. of knowledge of MRSA, poor contact with residents with MRSA due to dementia or mental health, and economic challenges regarding increased care for resident with References MRSA as factors contributing to why hygiene guidelines are not always followed. Albrich W C, Harbarth S (2008). Health-care workers: Source, vector, or victim of MRSA? Lancet. Infectious Diseases, 8(5): 289–301 Andersson H, Lindholm C, Iversen A, Giske C G, Örtqvist Å, Kalin M, 5 Concluding remarks Fossum B (2012). 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