Carbapenem-resistant Enterobacterales (CRE) represent a serious infectious disease threat, severely limiting therapeutic options. Mortality rates associated with CRE infections, such as Klebsiella pneumoniae, are reported to be 3.7-6.5 times higher than those of infections caused by carbapenem-susceptible strains [1,2]. The extensive use of carbapenems has contributed to the rise in CRE infections in healthcare settings, leading to a public health crisis driven by antibiotic-resistant bacteria [3,4]. In Korea, the number of reported cases of CRE has increased 6.7 times from 2017 to 2023 [5]. High colonization rates of multidrug-resistant (MDR) bacteria lead to the increased use of broad-spectrum antibiotics, which in turn increases MDR bacterial colonization. Moreover, carbapenemase-producing Enterobacterales (CPE) can acquire additional resistance genes via horizontal gene transfer, further complicating treatment [6]. The plasmid-mediated carbapenemase enzymes also pose a risk of outbreaks within healthcare facilities, necessitating continuous surveillance and effective infection control measures [7,8].

As asymptomatic carriers can act as reservoirs for transmission, strategies involving active surveillance and isolation of patients newly admitted for CRE have been proposed to prevent outbreaks of CRE colonization [9]. Chitnis et al. demonstrated that active surveillance and subsequent isolation of carriers significantly reduced transmission in a long-term care hospital [10]. In Korean hospitals, where standard rooms typically accommodate 4-6 patients with a single bathroom, the risk of transmission through contact among patients in the same room is higher. Considering that resistant bacteria are associated with higher mortality rates than susceptible strains, an outbreak of CRE may result in more severe consequences than those caused by susceptible bacteria.

The study hospital, operated by the Seoul Metropolitan Government, includes a ward dedicated to homeless patients for public health purposes. Many patients admitted to this ward live without family, are chronic alcoholics, or have not previously sought hospital care, as well as those re-transferred from long-term care facilities after previous hospitalization. The patient population varies widely, encompassing cases ranging from trauma to newly diagnosed cancer, and is not limited to specific departments. Up to six patients may share a single room. As there has been no research on homeless populations in Korea, an analysis of the current situation is necessary to establish appropriate infection control strategies for CRE. This study aimed to analyze the impact of active surveillance for CRE in a homeless ward. Additionally, risk factors for acquiring CRE among hospitalized patients were identified.

1. Study design

This retrospective study compared CRE incidence in the homeless ward of a hospital with approximately 800 beds before and after the introduction of active surveillance, from October 1, 2023, to May 31, 2024. Targeted active surveillance for CRE in the ward was conducted from January 22, 2024. CRE incidence was also compared with that of general wards, excluding intensive care units and the homeless ward, during the same period. Additionally, we analyzed the risk factors for CRE colonization and in-hospital mortality among hospitalized patients during the study period.

The homeless ward includes 26 beds across one single-patient room, one three-patient room, one four-patient room, and three six-patient rooms, and accommodates patients from various departments in a shared space. Owing to the ward’s relatively small size and following a two-month CRE outbreak in November and December 2023, we proactively implemented active surveillance to prevent future outbreaks. All newly admitted patients, including those transferred from other wards such as intensive care units, underwent CRE examination through rectal swabs. All admitted homeless patients were included in the analysis, and only the calculated CRE incidence, without patient information, was used from the hospital infection control records for the general wards. The study was approved by the Institutional Review Board of Boramae Medical Center (No. 20-2024-35). The requirement for written consent was waived owing to the retrospective nature of the study.

2. Infection control strategies for CRE

CRE was defined as Enterobacterales resistant to any carbapenem [11]. Patients were not preemptively isolated in single-patient rooms after the CRE examination due to limited space; however, contact precautions were followed. Patients confirmed to have CRE in any clinical specimen, whether CPE or not, were isolated in single-patient rooms whenever possible, or in a cohort when they had the same genotype. Follow-up rectal CRE examinations for colonized patients were conducted at 3- to 7-day intervals until three consecutive negative results were obtained. When two or more cases were confirmed in the same room during the same week, this was defined as an outbreak, and rectal swab screening was performed on close contacts and other patients in the same room. Active surveillance for other antibiotic-resistant bacteria, such as vancomycin-resistant enterococci or methicillin-resistant Staphylococcus aureus, was not conducted in this ward. There were no changes in other strategies, such as environmental cleaning methods and intervals, before and after implementation.

3. Clinical characteristics and outcomes

The following clinical data of hospitalized patients in the ward were collected from electronic medical records: age, sex, and underlying diseases (e.g., hypertension, diabetes mellitus, malignancy, chronic heart disease, chronic liver disease, chronic kidney disease, chronic pulmonary disease, and neurological disorders). Chronic heart disease included cardiovascular disease and chronic heart failure; chronic liver disease was defined by the presence of liver cirrhosis; chronic renal disease was defined as a glomerular filtration rate of less than 60 mL/min/1.73 m₂; and chronic pulmonary disease encompassed conditions such as tuberculosis-destroyed lung, chronic obstructive pulmonary disease, and bronchiectasis, all characterized by impaired lung function affecting daily activities, as described previously [12,13]. Additionally, factors such as previous hospitalization in the past year, transfer from other hospitals, previous CRE colonization, and antibiotic use in the past three months were considered. We determined whether patients with CRE colonization were identified through active surveillance upon admission or through cultures of clinical samples such as sputum, urine, or blood during the hospital stay. The total hospital days for the patients, presence of CRE infection, type of carbapenemase, presence of colonization by other MDR bacteria such as methicillin-resistant S. aureus, vancomycin-resistant Enterococcus, carbapenem-resistant Acinetobacter baumannii, and carbapenem-resistant Pseudomonas aeruginosa, and in-hospital mortality were reviewed. MDR bacterial colonization was assessed by reviewing the culture results of all clinical samples collected during hospitalization.

4. CRE screening programs and carbapenemase gene testing

CRE screening was performed according to a modified Centers for Disease Control and Prevention protocol [14]. Each rectal swab was inoculated into trypticase soy broth and incubated for 6-12 h. The broth culture was then vortexed and subcultured on MacConkey agar (BANDIO) containing an imipenem disk and/or ChromID® CARBA chromogenic agar (bioMérieux, Marcy-l’Etoile). The plates were incubated overnight at 35℃±2℃ under ambient air conditions. Suspicious Enterobacterales colonies were detected based on specific phenotypic features, and identification and antimicrobial susceptibility testing was confirmed using a VITEK® 2 automated system (bioMérieux, Marcy-l’Etoile). For CRE-positive specimens, the Xpert® Carba-R Assay (Cepheid) was performed according to the manufacturer’s instructions.

5. Statistical analysis

The incidence of new CRE colonization in a homeless ward was compared before and after the implementation of active surveillance using Poisson regression analysis [15]. Furthermore, the clinical characteristics of the patients with and without CRE colonization were compared. According to the results of the Shapiro–Wilk test, either the Student’s t-test or Mann–Whitney U-test was used to compare continuous variables. The Chi-square test or Fisher’s exact test was used to compare categorical variables. Statistical significance was set at P<0.05. Independent risk factors for colonization of CRE and in-hospital mortality were analyzed with multivariate analysis using backward stepwise logistic regression, with P=0.05 as the cut-off value for removing variables. Multicollinearity was checked using variance inflation factors, with the cut-off set at 5. All analyses were performed using PASW Statistics for Windows (version 29.0; IBM SPSS Inc.) and R software version 4.3.1 (http://www.R-project.org).

1. Incidence of CRE colonization cases and outbreaks

Fig. 1 shows the monthly incidence of CRE colonization in the homeless and general wards, except intensive care units. Eighteen new CRE cases were identified in the homeless ward during the study period. Before the implementation of active surveillance, 10 new cases of CRE colonization were identified, including two outbreak events over a 3-month period. After active surveillance was introduced, eight cases were identified over 4 months, with no outbreak events. The CRE incidence rate decreased from 1.149 per 1,000 patient-days to 0.815 per 1,000 patient-days; however, this change was not statistically significant (rate ratio, 0.986; 95% confidence interval (95% CI), 0.389-2.496; P=0.976). The overall incidence rate of CRE colonization remained higher in the homeless ward than in the general wards.

Figure 1. (A) Monthly newly detected cases of carbapenem-resistant Enterobacterales (CRE) in the homeless ward and (B) comparison of incidence rates (cases per 1,000 patient-days) between the homeless and general wards (except intensive care units) before and after the implementation of active surveillance.

Until the second month following the intervention, three index cases were identified from clinical samples (urine, sputum, and intra-abdominal drain). Of these, two patients were hospitalized before surveillance began, and one patient was identified in March from a clinical sample despite testing negative during surveillance. In contrast, the remaining five cases were detected through active surveillance, with all cases from April onwards identified via surveillance examinations. All cases were confirmed to be CPE: K. pneumoniae carbapenemase (KPC)-producing K. pneumoniae (five cases, 62.5%), New Delhi metallo-β-lactamase-producing Escherichia coli (two cases, 25.0%), and OXA-producing K. pneumoniae (one case, 12.5%). Among these, four patients (50.0%) developed CPE bacteremia, and two patients (25.0%) died during hospitalization.

2. Characteristics of patients based on CRE colonization

Table 1 presents the characteristics of the study population. From October 2023, 18 patients had CRE and 106 had non-CRE in the homeless ward. The median age of the CRE group was 69.5 years, which was higher than that of the non-CRE group of 62.0 years (P=0.024). Most patients (97.6%) in the homeless wards were male. A history of antibiotic exposure within the past 3 months was more common in the CRE group than in the non-CRE group (22.2% vs. 3.8%, P=0.009).

Table 1 . Comparison of characteristics of patients admitted to the homeless ward based on CRE colonization

	CRE n=18	non-CRE n=106	Total n=124	Univariate analysis			Multivariate analysis
				OR (95% CI)	P		aOR (95% CI)	P
Age, median (IQR)	69.5 (65.0-75.0)	62.0 (55.0-69.0)	64.0 (55.0-70.0)	1.061 (1.008-1.117)	0.024		1.071 (1.014-1.132)	0.014
Sex, male (%)a	18 (100.0%)	103 (97.2%)	121 (97.6%)
CRE colonization previous three months, n (%)a	3 (16.7%)	0 (0.0%)	3 (2.4%)
Antibiotics exposure previous three months, n (%)	4 (22.2%)	4 (3.8%)	8 (6.5%)	7.286 (1.635-32.465)	0.009		6.796 (1.215-38.029)	0.029
Hospitalization previous year, n (%)	8 (44.4%)	29 (27.4%)	37 (29.8%)	2.124 (0.764-5.909)	0.149
Underlying diseases, n (%)
Hypertension	9 (50.0%)	40 (37.7%)	49 (39.5%)	1.643 (0.529-5.112)	0.435
Diabetes mellitus	7 (38.9%)	28 (26.4%)	35 (28.2%)	1.773 (0.601-4.965)	0.421
Malignancy	8 (44.4%)	21 (19.8%)	29 (23.4%)	3.238 (1.115-9.248)	0.048
Heart	1 (5.6%)	19 (17.9%)	20 (16.1%)	0.269 (0.015-1.442)	0.331
Kidney	5 (27.8%)	8 (7.5%)	13 (10.5%)	4.712 (1.267-16.458)	0.030
Liver	4 (22.2%)	20 (18.9%)	24 (19.4%)	1.229 (0.322-3.864)	0.992
Pulmonary	5 (27.8%)	21 (19.8%)	26 (21.0%)	1.557 (0.459-4.651)	0.649
Neurological	6 (33.3%)	20 (18.9%)	26 (21.0%)	2.150 (0.680-6.276)	0.280
Outcomes, n (%)
Other MDR colonizationb	10 (55.6%)	15 (14.2%)	25 (20.2%)	7.583 (2.604-23.031)	<0.001		7.168 (2.224-23.096)	0.001
Hospital days, median (IQR)	28.5 (22.0-55.0)	9.0 (5.0-19.0)	10.5 (6.0-24.5)	7.168 (2.224-23.096)	0.007
In-hospital mortality	3 (16.7%)	6 (5.7%)	9 (7.3%)	3.333 (0.651-14.139)	0.241

^aStatistical comparison was not possible due to the small number of cases.

^bMDR bacterial colonization was assessed by reviewing culture results of all clinical samples during hospitalization. Colonization with methicillin-resistant Staphylococcus aureus, vancomycin-resistant enterococcus, carbapenem-resistant Acinetobacter baumannii, or carbapenem-resistant Pseudomonas aeruginosa was considered colonization of MDR bacteria if any one of these was detected.

Abbreviations: CRE, carbapenem-resistant Enterobacterales; OR, odds ratio; aOR, adjusted odds ratio; CI, confidence interval; SD, standard deviation; MDR, multidrug-resistant; IQR, interquartile range.

Regarding underlying comorbidities, chronic kidney disease was more prevalent in the CRE group (27.8%) than in the non-CRE group (7.5%; P=0.030). The median hospitalization period for the CRE group was 28.5 days (interquartile range (IQR) 22.0-55.0), significantly longer than the 9.0 days (IQR 5.0-19.0) in the non-CRE group (P=0.007). During hospitalization, co-colonization with MDR bacteria was more common in the CRE group (55.6%) than in the non-CRE group (14.2%) (P<0.001). In-hospital mortality was higher in the CRE group than in the non-CRE group, but the difference was not statistically significant (16.7% vs. 5.7%; P=0.241).

Multivariate analysis showed that CRE colonization was significantly associated with age (adjusted odds ratio (aOR), 1.071; 95% CI, 1.014-1.132; P=0.014), previous antibiotic exposure (aOR, 6.796; 95% CI, 1.215-38.029; P=0.029), and co-colonization with MDR bacteria (aOR, 7.168; 95% CI, 2.224-23.096; P=0.001).

3. Risk factors for in-hospital mortality

When comparing the 18 patients who died and 106 who survived during the study period (Supplementary Table 1), chronic lung disease was more common in the non-survivor group (non-survivors vs. survivors: 55.6% vs. 18.3%; P=0.026). Additionally, CRE infection, mostly accompanied by bacteremia, except for one case of pneumonia, was significantly more prevalent in non-survivors (33.3% vs. 3.5%; P=0.003). Non-survivors also had higher rates of colonization by other MDR bacteria than survivors (66.7% vs. 16.5%; P=0.001). Chronic lung disease (aOR, 5.094; 95% CI, 1.086-23.903; P=0.039), CRE infection (aOR, 8.528; 95% CI, 1.360-53.475; P=0.022), and longer hospital stay (aOR, 1.019; 95% CI, 1.003-1.035; P=0.023) were independently and significantly associated with in-hospital mortality.

This study describes the incidence of CRE colonization in the homeless ward, which includes multiple shared rooms, of an acute care hospital in Korea, and the short-term effects of active surveillance for CRE in the ward. After implementing active surveillance, a small number (one to two cases) of CRE colonizers were identified monthly from newly admitted patients. No outbreaks occurred within the first four months of active surveillance. Among the new CRE cases, all were CPE and 62.5% were KPC-producing K. pneumoniae, which aligns with the recent epidemiology in Korea [16]. The absence of new outbreaks suggests that active surveillance and isolation on admission may have prevented the contact transmission of hidden CRE colonizers in this population.

To our knowledge, this is the first report of active surveillance in a ward for homeless patients in Korea. While previous studies have highlighted the importance of active surveillance in managing CRE in healthcare settings, most efforts have focused on intensive care units [17,18]. This study demonstrated the effectiveness of active surveillance in a ward where high-risk patients share rooms. Previous studies have shown that CRE colonization is associated with CRE infection and prolonged hospitalization [19,20]. Similarly, our findings indicate that, in addition to CRE infections, coexisting lung diseases and extended hospital stays were associated with higher mortality rates, which is consistent with earlier studies [21-23].

Age, previous antibiotic exposure, and underlying chronic kidney disease were identified as risk factors for CRE colonization, which has been documented in other studies [9,24]. However, research challenges the common belief that patients with low socioeconomic status have lower colonization rates of resistant bacteria owing to their limited access to hospital care and antibiotics [25]. In our study, the CRE incidence rate in the homeless ward was higher than that in the general wards, although direct comparison was limited because the general wards did not implement active surveillance (Fig. 1B). Although few studies have investigated CRE colonization rates in homeless populations in Korea, prior studies conducted in other countries, primarily among refugees and asylum seekers, have highlighted an increase in antibiotic-resistant E. coli and carbapenem-resistant A. baumannii among them [26,27]. A single-institution study in Korea analyzing patients with tuberculosis among the homeless population reported that 45.8% of patients had prior exposure to shelters or healthcare facilities [28]. In addition, our study found that 29.8% of homeless patients had a recent hospitalization history, suggesting that the risk of exposure to resistant bacteria in this population is not negligible. Contributing factors may also include poor hygiene and crowded living conditions [25]. In highly endemic settings where homeless patients with various conditions share rooms, active surveillance may serve as a potentially useful strategy for infection control [29].

In this study, surveillance was performed once upon admission without routine follow-up screenings, and clinical cultures were performed as needed. Using this approach, only one case of CRE acquisition was confirmed after the initial surveillance examination. Despite the short duration of this study, no additional outbreaks occurred. Further research is required to assess whether a more intensive strategy, including regular CRE screening for patients with specific risk factors, is necessary for effective infection control [9,30]. Additionally, conducting a cost-effectiveness analysis of different strategies, such as one-time versus routine surveillance, could offer valuable insights into optimizing infection control measures.

A major limitation of our study is the small number of CRE cases and the short study period, both of which may limit the generalizability of our findings to the broader homeless population in Korea. Given the nature of the homeless patient population, the reliability of information regarding antibiotic use and medical history may also be compromised. However, considering the diverse characteristics of the patients, a CRE outbreak could result in significant harm. Therefore, in Korea, where the use of single-patient rooms is limited, the prevention of CRE outbreaks through active surveillance is important for maintaining infection control in shared room settings. Additionally, although we compared CRE incidence between the homeless and general wards, it is important to note that the general wards did not undergo surveillance, making direct comparison challenging.

In conclusion, although there was no significant change in the incidence of CRE colonization, no CRE outbreaks occurred in the homeless ward of an acute care hospital following the implementation of active surveillance. CRE colonization was associated with older age, previous antibiotic exposure, and colonization by other MDR bacteria.

Supplementary material can be found via https://doi.org/10.14192/kjicp.2024.29.2.128.

The authors would like to thank the clinicians and nurses in the homeless ward for their cooperation in conducting the active surveillance.

The authors have no potential conflict of interest to disclose.

None.

Conceptualization: EL. Data curation: DHS & JEY. Formal analysis: DHS & EL. Investigation: JEY & IE. Methodology: EL. Project administration: EL & MSH. Supervision: EL. Writing: DHS, NK, & EL. Review and editing: all authors.