Multidrug-resistant organisms (MDROs) are micro-organisms that are resistant to one or more classes of antimicrobial agent.1 Infections caused by MDROs often fail to respond to standard therapy and require treatment with “big gun” antibiotics, which may be associated with higher toxicity and cost. Infection with MDROs leads to prolonged illness and higher mortality than more common infections. Discharging asymptomatic colonisers from hospital to the community, especially to long-term care facilities, may increase the risk of transmission among community residents.2

In Hong Kong, residential care homes for the elderly (RCHEs) are a heterogeneous group of institutions providing different levels of care for elderly people, who, for personal, social, health or other reasons, can no longer live alone or with their families. Around 9% of the elderly population in Hong Kong requires residential care. As of March 2015, there were approximately 750 RCHEs providing over 79 000 residential places for elderly people.3

Long-term care facilities are an important reservoir for MDROs.4 Risk factors from reported cases of MDRO infection and colonisation include use of indwelling medical devices, frequent antibiotic usage and prolonged hospitalisations, all of which are common among residents of long-term care facilities.5

Methicillin-resistant Staphylococcus aureus (MRSA) is defined as S aureus being resistant to penicillinase-resistant penicillins (eg, methicillin, oxacillin or cloxacillin) and cephalosporins. As a common pathogen causing health care–associated infections, MRSA has placed a substantial burden on health care resources.6 In Hong Kong, MRSA is endemic.7 More than 40% of S aureus isolated in public hospitals are MRSA. Half of the MRSA carriers among hospitalised patients aged ≥65 years were admitted from RCHEs.8 Prevalence of MRSA among long-term care residents in Europe ranged from 8% to 25%.9 10

Multidrug-resistant Acinetobacter (MDRA) is defined as a pathogen showing concomitant resistance to fluoroquinolones, carbapenems, aminoglycosides, cephalosporins, and beta-lactam with or without beta-lactamase inhibitors. Among hospitalised patients,11 especially in intensive care units,12 13 MDRA is an important pathogen. It can cause pneumonia, blood stream infection, skin and soft tissue infection, and urinary tract infection.14 15 Data on MDRA prevalence among RCHE residents in Hong Kong are limited.

Vancomycin-resistant Enterococcus (VRE) is defined as Enterococcus faecalis or Enterococcus faecium which is resistant to vancomycin. Carbapenemase-producing Enterobacteriaceae (CPE) is Enterobacteriaceae resistant to the carbapenem class of antibiotics. Compared with Western countries, incidence of infection with emerging MDROs such as VRE and CPE is relatively low in Hong Kong16; however, in 2013, there were outbreaks of VRE among geriatric patients in public hospitals in Kowloon. These outbreaks raised concerns about the discharge of asymptomatic carriers back to RCHEs that may lead to further outbreaks, particularly if there is a lapse in infection control practice in RCHEs.17

There have been few local studies on the prevalence of MDRO colonisation among RCHE residents.18 19 A better understanding of local MDRO epidemiology in RCHE settings is important for planning surveillance and control strategies to prevent increases in MDRO prevalence among RCHE residents.

The present survey aimed to estimate the prevalence of MDROs with public health impacts such as MRSA, MDRA, VRE and CPE among RCHE residents in Kowloon City District, Hong Kong, and to examine risk factors associated with MDRO colonisation.

A point prevalence survey was conducted to estimate the MDRO burden among residents in participating RCHEs and associated factors of MDRO carriage. All RCHEs with a capacity of 30 residents or more in the catchment area of Queen Elizabeth Hospital and Kowloon Hospital in Kowloon City District were included. All residents aged ≥65 years who were in the RCHE at 9 am (the reference time) on the survey day, and consented to participate were included.

A list of all 60 RCHEs in the target area was retrieved. The RCHEs were stratified by home type: ‘non-private’ for government-subsidised homes and ‘privately run’ for profit-making homes. Stratified single-stage cluster sampling was applied to select a representative sample of residents from RCHEs at the ratio of 1:8, which was similar to the ratio of residential beds provided by non-private to privately run homes.

Sample size estimation was based on the primary objective of the study, which was to determine the prevalence of MDROs (MRSA, MDRA, VRE and CPE) in RCHEs. Prevalence of MRSA colonisation was estimated to be 18.7% based on a local study in RCHEs in 2011.20 Since no prior information on the design effect and intraclass correlation coefficient was available, a conservative approach was taken. The intraclass correlation coefficient was set at 0.025 and the design effect was set at 2, based on estimates from a previous local study on infections in RCHEs.21 Assuming the 95% confidence interval (CI) of MRSA prevalence estimated from current study to be ±3.74% (relative precision [ie, margin of error] was 3.74/18.7(%) = 0.2), the sample size required was 836.22

Sample size was not estimated for the prevalence of MDRA, VRE, or CPE. For MDRA, local prevalence in RCHEs was not available. From experience in hospitals, it was expected that the prevalence of MDRA would be lower than that of MRSA and higher than that of VRE.

From experience in hospitals and from admission screening data for VRE and CPE, VRE was expected to be very uncommon and CPE was expected to be even rarer in RCHEs. Based on information from the Infection Control Branch, Centre for Health Protection, which keeps statistics on patients discharged from hospital to RCHEs, there were a total of 40 VRE carriers discharged from hospitals to RCHEs in Kowloon City District from January to September 2013. The RCHE bed capacity in Kowloon City District was 7796 at the end of September 2013; therefore, a rough estimation was made for the prevalence of VRE in these RCHEs of 0.51% (40/7796). On the basis of the estimated sample size for measuring MRSA prevalence in RCHE (ie, 836) the study has the power to detect VRE prevalence with point estimate of 0.51% (95% CI=0%-1.20%), with a relative precision of 1.34.

As the median bed capacity in RCHEs in Kowloon City District is 74, assuming 60% of RCHE residents would agree to be surveyed, a total of 1400 residents from 19 RCHEs needed to be recruited. Assuming a response rate from RCHEs of 60%, at least 32 RCHEs needed to be invited to join the study.

Invitation letters were sent to RCHEs to introduce the survey and invite them to join. For RCHEs that agreed to participate, the survey team visited the RCHE twice. The first visit was to obtain consent from residents (consent day). The second visit was to collect information and specimen from consenting residents on a single day between September and December 2015 (survey day). The RCHEs were allowed to select the survey day freely.

Residents who consented but were absent on the survey day were excluded from the survey. Potential additional residents (including those absent on the consent day but present on the survey day) were invited to join on the survey day.

A survey form was used to collect RCHE information including home type and resident information including demographics, medical history, use of indwelling catheter, history of hospitalisation, and history of antimicrobial use over the previous year. Resident information was extracted from medical records stored in RCHEs. Nearly all residents were under the care of the Community Geriatric Team of the Hospital Authority. The Community Geriatric Team records were comprehensive, including medical history, hospitalisation to public hospitals, and medication prescribed by public hospitals. Occasionally, residents would seek help from private doctors. The RCHEs keep records of private consultations, including date of medical consultation, name of doctor consulted, and medication prescribed by private doctors. We extracted the best available data from these two sources. Functional status of residents was assessed by the survey team using the Katz index.23 The Katz index assesses independence in activities of daily living on a 7-point Likert scale from 0 to 6, where 6 points implies total independence. The survey team consisted of doctors and nurses who had experience working in infection control for at least 1 year. Inter-rater reliability for the Katz index among members of the team during the pilot survey was assessed using the Fleiss kappa coefficient.

For each consenting resident, the survey team took the following samples: nasal swab for MRSA, axillary swab for MRSA and MDRA, stool (or rectal swab in cases when stool could not be collected) for VRE, CPE, and MDRA. A standard survey protocol on swab taking was developed and survey team members were trained for specimen collection. For the rectal swab, faeces should be evident on the swab. All specimens were sent to the Microbiology Laboratory of Queen Elizabeth Hospital for culture.

One third of the MRSA-positive samples were selected at random for molecular typing. All MDRA, VRE and CPE samples were subjected to molecular typing.

For missing data identified in the survey forms, the relevant RCHE was contacted shortly after the survey for remedial work. Double data entry by two different staff members was adopted to minimise data entry error. To ensure data quality, 5% of the data were selected from the cleansed dataset to check against the hard copies.

The nasal, axillary, and rectal swab specimens collected were directly inoculated onto agar plates. Rectal swabs were visually inspected for presence of faecal materials. For faecal samples, sterile swab was used to swab a viscous portion of specimens and to inoculate onto agar plates.

Screening for MRSA was performed using chromID MRSA agar (bioMérieux, Marcy-l‘Étoile, France). The chromID MRSA agars were incubated at 35 ± 2°C for 24 hours. Green colonies were picked for further characterisation by Gram stain, coagulase and Staphaurex latex agglutination test (Thermo Fisher Scientific, Waltham [MA], US). Methicillin susceptibility was confirmed by cefoxitin disk diffusion test.

Typically, MDRA is characterised by Gram stain, biochemical reactions, and Vitek 2 (bioMérieux) with Gram-negative ID cards. Selective cultivation of MDRA was performed using CHROMagar Acinetobacter agars with multiple-drug resistant selective supplement (CHROMagar, Paris, France) which were incubated at 35 ± 2°C for 48 hours. Resistance to fluoroquinolones, carbapenems, aminoglycosides, cephalosporins, and beta-lactams was confirmed by disk diffusion test.

Surveillance for VRE was performed using chromID VRE (bioMérieux) agar, which were incubated at 35 ± 2°C for 48 hours. Suspected colonies were characterised by Gram stain, biochemical tests, and Vitek 2 with Gram-positive ID cards. Vancomycin susceptibility was confirmed by disk diffusion test and E-test.

chromID CARBA (bioMérieux) was used to selectively recover CPE. The chromID CARBA agars were incubated at 35 ± 2°C for 24 hours. Gram stain, biochemical tests, and Vitek 2 with Gram-negative ID cards were used for identification of Enterobacteriaceae. Non-susceptibility to meropenem, imipenem and ertapenem were confirmed using E-tests. Presence of carbapenemase production was screened for using a modified Hodge test with meropenem and ertapenem and a combined-disc test with boronic acid and ethylenediaminetetraacetic acid. Results were confirmed with GeneXpert (Cepheid, Sunnyvale [CA], US) Carba-R assay. All disk diffusion tests were performed according to the Clinical and Laboratory Standards Institute.24

Molecular typing was performed using DiversiLab version 3.6.1 (bioMérieux). Typing procedures were performed according to the manufacturer’s instructions. The cluster analysis was performed according to the guidelines provided by the manufacturer using Pearson’s correlation and the Kullback-Leibler method. Isolates were categorised as indistinguishable, similar, or different.

R software (ver. 3.2.0; https://www.r-project.org) was used for statistical analysis. For all analyses, statistical significance was defined as P<0.05. Descriptive statistics were computed using all data collected. The “survey” package (version 3.30-3) in R was used to calculate the prevalence of MDRO carriage adjusted for cluster sampling. The prevalence of MDRO carriage among all surveyed RCHEs was calculated using the “svyciprop” function from the “survey” package, which calculates the prevalence as the sample-weighted estimator of the proportion.25 The CI was calculated by a procedure closely related to that proposed by Breeze for use in the United Kingdom General Household Survey26 which is calculated as a binomial probability using the Wilson interval method,27 followed by a logit transform.25 Prevalence of MDRO carriage among individual RCHEs was calculated by dividing the number of residents positive for MDRO culture by the total number of residents surveyed in that particular RCHE. Percentages for other study variables were calculated similarly. Logistic regression with adjustments for cluster sampling was performed using “svyglm” function from the “survey” package to identify risk factors for MRSA carriage. Variables were included for multivariate analysis if P<0.25 in univariate analysis; or if variables had been considered as risk factors of infection in previous studies, such as mobility status,28 use of medical devices,29 presence of wound,29 home size,29 sex,30 and recipient of Governmental Allowance (as a surrogate measurement of socio-economic status).31 Selected variables were incorporated into the multivariate regression model in descending order of effect size estimated from the univariate regression. Variables were not included to multivariate regression model if the model with additional variable showed no statistical significance in the residual sum of squares reduction.

Grouping of quantitative variables for regression modelling was based on following criteria: (i) RCHE capacity was stratified into two groups by median RCHE capacity; (ii) resident age was grouped for every 10 years; (iii) Katz index was grouped into the reference group (6 points), low dependence (3-5 points) and high dependence (0-2 points); (iv) RCHE length of stay stratified into two groups by median RCHE length of stay among surveyed residents; and (v) hospital length of stay stratified into two groups by mean length of stay reported by the Hospital Authority for 2014-2015.32

The survey was conducted in a linked and anonymous manner to avoid unnecessary anxiety or stigmatisation due to positive MDRO carriage status.33 Measures were taken during the process of preparation, specimen collection, and data processing and storage to ensure protection of participants’ anonymity.

We invited 56 RCHEs (50 privately run and 6 non-private) among the 60 RCHEs in Kowloon City District to participate in the study. Of these, 20 RCHEs joined the study (Table 1). The number of residents of the recruited RCHEs ranged from 25 to 265.

A pilot survey was conducted in one RCHE from which 45 residents joined. The Fleiss kappa coefficient of the total Katz index was 0.977, and scores for individual items ranged from 0.972 to 1, suggesting good inter-rater reliability among all members of the survey team.

Including those who participated in the pilot, 1520 eligible residents were invited and 1092 consented to participate in this survey (consent rate, 71.8%). Consent could not be obtained from the remaining 428 residents, either because they refused or their relatives or guardians could not be contacted.

On the survey days for selected RCHEs, 10 residents who had previously given consent refused to participate, 27 left the RCHE for personal business, 24 were hospitalised, and three were attending medical appointments. The remaining 1028 residents completed the survey.

Swabs were taken from 1028 residents on a single day (survey day) for each RCHE during the 3-month period from mid-September to mid-December 2015 (1026 nasal swabs, 1027 axillary swabs, 373 stool and 654 rectal swabs), achieving a survey rate of 67.6%.

Among the 1028 respondents, 411 (40.0%) were men and 617 (60.0%) were women. The median age was 85 years (range, 65-104 years) and more than half (55.3%) were aged ≥85 years. The majority were of Chinese ethnicity (98.0%). The median length of stay in RCHE was 1.8 years (range, 1 day to 23.4 years). Table 2 shows the majority did not regularly use any medical devices (85.9%) or have any wounds (95.4%). Almost all respondents (99.8%) had underlying chronic diseases. The most common disease was hypertension (72.8%) followed by dementia (38.3%), stroke (31.3%), diabetes (26.8%), and ischaemic heart disease (22.0%). Over half of respondents (58.6%) had a history of hospitalisation in the past 12 months with a mean of 2.9 episodes of hospital admission (range, 1-16 episodes). More than half of respondents (60.7%) had used antibiotics in the past 12 months. The most commonly used antibiotics were amoxicillin/clavulanate (50.4%) followed by levofloxacin (12.9%) and piperacillin/tazobactam (7.2%). Most respondents (90.6%) were partially or totally dependent in activities of daily living, with a Katz index of <6. Of the respondents, 1.36% had a history of known MDRO in the past 12 months.

Out of 1028 residents, 1027 were tested for MRSA with 282 positive results (prevalence adjusted for cluster sampling: 30.1%; 95% CI=25.1%-35.6%). All 1028 residents were tested for MDRA and three carried MDRA (prevalence adjusted for cluster sampling: 0.6%; 95% CI=0.1%-4.1%). A total of 1027 residents were tested for VRE and CPE; all tested negative. Culture positive rates of MRSA for nasal swab and axillary swab were 22.1% and 10.3%, respectively. Culture positive rates for MDRA for axillary swab, rectal swab, and stool were 0.1%, 0.2%, and 0.5%, respectively.

All participating RCHEs (n=20) had MRSA carriers with MRSA prevalence ranging from 13.2% to 57.1% (Table 3). There were no common MRSA sources revealed by the diversified molecular typing of 54 patterns (no band difference between strains within a pattern) and 12 groups (1 band difference between strains within group).

Three residents living in the same RCHE carried MDRA. The prevalence of MDRA at this RCHE was 11.5% (95% CI=4.00%-28.98%). Strain typing revealed that all three likely belonged to the same MDRA strain, as the band patterns were identical.

Compared with the 742 MDRO non-carriers, univariate analysis revealed several factors associated with MDRO positivity (Table 4). Inclusion of RCHE capacity, governmental allowance, and indwelling urinary catheter in the multivariate logistic regression model did not provide statistically significant decrease in residual sum of squares when compared with the simpler model; therefore, the simpler model was used. This model revealed that residents from privately run RCHEs were associated with MRSA colonisation and non-Chinese residents were associated with MRSA carriage with borderline significance.

Owing to the low participation rate of non-private RCHEs, an additional regression model was developed with residents from only privately run RCHEs, to explore the association of different risk factors with MRSA colonisation. After comparison, no differences in terms of direction, effect size, or statistical significance were observed between the two models.

In the present study, the survey revealed a high prevalence of MRSA among RCHE residents in Hong Kong. The prevalence of MDRA, however, remained low in the same population, and VRE or CPE was not found among surveyed residents.

All RCHEs surveyed had MRSA carriers. The adjusted prevalence of MRSA colonisation was 30.1%, which is similar to that of another survey conducted in RCHEs in Hong Kong Island during the same period of time (32.2%).34 Prevalence of MRSA was much higher than that found in previous studies in 2005 (2.8%)19 and in 2011 (21.6%).35 Internationally, MRSA prevalence in Hong Kong is similar to that in the US (31%),36 but higher than that in nursing home studies in the United Kingdom (4.7%)37 and in Shanghai, China (10.6%).38

The adjusted prevalence of MDRA was 0.6%. This is similar to a local hospital study conducted in 2014, which recorded a prevalence of multidrug-resistant Acinetobacter baumannii of 0.57%.39 As all three cases of MDRA were found in the same RCHE with identical molecular typing, we suspected a common source for the three carriers. We visited the RCHE and encouraged staff to implement better infection control practices. There were no subsequent outbreaks reported. Internationally, the prevalence of MDRA is much lower than that reported in studies from the US (prevalence of multidrug-resistant A baumannii was 15.0%)40 and Australia (prevalence of multidrug-resistant A baumannii was 5.2%).41

In RCHEs, the prevalence of MRSA is rising rapidly, and that of MDRA has the potential to rise. Thus, infection control practice in RCHEs should be enhanced. Early identification of residents carrying MDRO enables RCHE staff to implement enhanced infection control practices such as early isolation or cohorting. Hand hygiene protocols should be followed carefully by health care workers in RCHEs, especially when handling patients’ food or medication; after napkin rounds; and before and after nursing care processes.42 Environmental hygiene measures, such as regular cleansing and disinfection of residents’ immediate environment and frequently touched areas, are of similar importance.43

The present study identified no VRE or CPE carriers from 373 stool and 654 rectal swabs of the residents screened. This echoes an earlier study of 28 RCHEs in Hong Kong Island from July to August 2015.34 Among 1408 subjects screened in that study, a single resident had CPE and VRE was not detected in any screened specimens.

To contain the spread of VRE and CPE among residents in RCHEs, current practice is to inform the RCHE before a VRE or CPE carrier is planned to be discharged from hospital. The RCHE staff members are recommended to enhance infection control practices, to use designated equipment with the carrier, and to adopt modified contact precaution when providing care to the carrier. This strategy has been successful; no outbreaks have been detected among RCHEs receiving VRE or CPE carriers, and the prevalence of VRE and CPE remains low in these RCHEs. Extra resources are needed if a similar strategy is adopted to control further increases in the prevalence of MRSA and MDRA.

In the present study, residents of privately run RCHEs were more likely than residents of non-private RCHEs to be carriers of MRSA. This could be due to privately run RCHEs being more resource-limited, as reflected by the typically lower staff-to-residents ratio.44

The present study also found that MRSA colonisation was more common in non-Chinese residents than in Chinese residents. This is consistent with previously published research.45 To mitigate this, future infection control training should raise awareness among RCHE staff of this issue and to adopt adequate infection control measures for Chinese and non-Chinese residents alike.

Increased age, use of medical device, and previous MRSA colonisation or infection are risk factors that have been previously reported to be associated with MRSA colonisation.46 However, the present study did not show any statistically significance differences between MRSA carriers and non-carriers by multivariate analysis. This could be due to the small sample size or selection bias in this study. A larger study is required to identify other risk factors.

There are some potential limitations to the present study. We conducted the survey in RCHEs in Kowloon City District. This may affect the generalisation of the results to RCHEs in the rest of Hong Kong. Among 56 RCHEs invited, 19 out of 50 privately run RCHEs and 1 out of 6 non-private RCHEs agreed to join the survey; 67.6% of residents from these RCHEs participated. The low participation rate of RCHEs may reduce the representativeness of study sample to the Hong Kong population of RCHE residents. We had no information on non-participating residents for baseline characteristics comparison. Self-selection bias cannot be excluded. The sample size required to accurately assess MRSA prevalence was estimated. The actual sample size may be insufficient for risk factor identification and effect size estimation. We extracted residents’ information from medical records kept by participating RCHEs; therefore, information bias due to measurement error cannot be eliminated, and missing data in the medical records may lead to bias. Prevalence of MRSA or MDRA may be underestimated as only nasal and axillary swabs were taken. Other sites such as wounds, catheter sites, groins or perianal region were not sampled. The MDRA detection sensitivity would be improved by using sterile sponges to sample multiple body sites.47

Emergence of MDROs is a global health threat and Hong Kong is not exempt. Residents of RCHEs are particularly vulnerable to MDRO colonisation or infection. Enhanced infection control is important to mitigate further increases in MDRO prevalence in RCHEs. The present study provides an understanding of the situation of MDROs in RCHEs. Further larger-scale studies on MDROs in Hong Kong are required to formulate a targeted infection control programme to prevent further spread of MDROs in the community.

Concept and design of study: All authors.
Acquisition of data: H Chen, KM Au, KE Hsu, CKC Lai, J Myint, YF Mak.
Analysis and interpretation of data: H Chen, KE Hsu.
Drafting of the article: H Chen, KE Hsu.
Critical revision of important intellectual content: H Chen, CKC Lai, J Myint, YF Mak, SY Lee, TY Wong, NC Tsang.

The authors thank colleagues of the Community Geriatric Assessment Team of Queen Elizabeth Hospital and Kowloon Hospital for their dedication and support. The authors also thank the health care workers of all participating RCHEs.

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

All authors have disclosed no conflicts of interest. All authors had full access to the data, contributed to the study, approved the final version for publication, and take responsibility for its accuracy and integrity.

The survey was approved by the Ethics Committee of Kowloon Central Cluster, the Hospital Authority, and the Department of Health. Written informed consent was obtained from all residents or from their relatives or guardians.

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