Impact of universal contact precautions and chlorhexidine bathing on the acquisition of carbapenem-resistant Enterobacterales in the intensive care unit: A cohort study

doi:10.21203/rs.3.rs-5023297/v1

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Impact of universal contact precautions and chlorhexidine bathing on the acquisition of carbapenem-resistant Enterobacterales in the intensive care unit: A cohort study

https://doi.org/10.21203/rs.3.rs-5023297/v1

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published 22 Nov, 2024

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Background

For the prevention of carbapenem-resistant Enterobacterales (CRE) acquisition in the intensive care unit (ICU), the effectiveness of universal contact precautions (UCP) and chlorhexidine gluconate (CHG) bathing is controversial.

Methods

With the aim of evaluating the effectiveness of UCP and CHG on CRE acquisition, this study was conducted in an ICU at a university-affiliated hospital in Seoul. Beginning in April 2017, all patients admitted to the ICU underwent CRE screening and surveillance tests weekly, and beginning in January 2018, UCP and CHG bathing were implemented for all patients. The pre-intervention period spanned from April to December 2017; the post-intervention period spanned from January 2018 to December 2019. The pre- and post- intervention CRE acquisition rates were then compared using Kaplan-Meier analysis and log-rank tests, and independent risk factors for CRE acquisition were analysed using Cox proportional hazard modelling.

Results

Of 1,747 patients, 35 acquired CRE during their ICU stay. Between the pre-intervention and post-intervention periods, the CRE acquisition rate did not differ significantly (p = 0.357). Additionally, multivariable Cox regression revealed that CRE acquisition was significantly associated with carbapenem exposure (adjusted hazard ratio [aHR] = 2.555, 95% confidence interval [CI] = 1.208–5.405, p = 0.013) and the presence of more than four patients colonised with CRE during their ICU stay (aHR = 2.639, 95%CI, 1.157–5.243, p = 0.019). However, UCP and CHG bathing had no significant association with CRE acquisition (aHR = 0.657, 95%CI = 0.301–1.433; p = 0.291).

Conclusions

UCP and CHG bathing did not affect the CRE acquisition rate in the ICU of a low-prevalence area. Therefore, a multimodal strategy including antibiotic stewardship is necessary for controlling the nosocomial spread of multidrug-resistant organisms.

Universal contact precautions

chlorhexidine bathing

carbapenem-resistant Enterobacterales

The global prevalence of carbapenem-resistant Enterobacterales (CRE) has risen significantly in recent years; in Korea specially, there was a notable rise from 15,369 cases in 2019 to 30,548 cases in 2022 according to reports from the Korea Disease Control and Prevention Agency [1]. The therapeutic options for CRE infections are limited, and there is a growing concern about resistance to newly developed beta-lactam and the beta-lactamase inhibitor combinations that constitute the primary treatment recommended in the Infectious Diseases Society of America’s guidelines [2, 3]. Recent data indicate that CRE infections are associated with higher mortality rates and prolonged hospital stays compared to those caused by carbapenem-susceptible Enterobacterales [4–6].

While previous studies have demonstrated the efficacy of universal gown and glove protocols (universal contact precautions [UCP]) for reducing the acquisition of multidrug-resistant gram-positive bacteria such as methicillin-resistant Staphylococcus aureus (MRSA), similar success has not been achieved for multidrug-resistant gram-negative bacteria including carbapenemase-producing Enterobacterales [7, 8]. However, those previous studies were conducted in intensive care units (ICUs) predominantly composed of single rooms, which limited their generalizability to environments where multibed rooms are common and there is therefore a higher risk of multidrug-resistant organism (MDRO) transmission.

Chlorhexidine gluconate (CHG) bathing has been investigated extensively to reduce infection caused by gram-positive bacteria such as MRSA and vancomycin-resistant Enterococci (VRE). However, studies on gram-negative bacteria such as CRE are limited [9]. Previous studies have only demonstrated a reduction in CRE colonisation among ICU patients before and after intervention [10, 11]. Therefore, evidence on whether UCP and CHG bathing in ICUs with multibed rooms can effectively reduce CRE acquisition remains scarce.

Beginning in April 2017, all patients admitted to the ICU of a single university-affiliated hospital in Seoul underwent CRE screening and surveillance tests at one-week intervals. UCP and CHG bathing were implemented for all patients beginning in January 2018; and, we analysed the effect of these interventions on the acquisition of CRE infection in the ICU.

This study was conducted in an ICU comprising four isolated single rooms and 22 multibed bays at a single university-affiliated hospital in Seoul. Beginning in April 2017, all patients admitted to the ICU underwent a CRE screening test on the day of admission, followed by subsequent surveillance tests conducted at one-week intervals. Beginning in January 2018, UCP and CHG bathing were implemented for all ICU patients. Infection control measures were reinforced due to the COVID-19 pandemic beginning January 2020. To assess the effect of UCP and CHG bathing on CRE acquisition, we designated the time interval from April 2017 to December 2017 as the pre-intervention period and from January 2018 to December 2019 as the post-intervention period. During these study periods, other infection control measures such as environmental cleaning and disinfection procedures were not altered.

A rectal swab specimen was obtained from the patient on the day of ICU admission, and culture was performed using selective media for CRE (CHROMagar™ Klebsiella pneumoniae carbapenemase, Hangang Inc., Korea). CRE identification and antibiotic susceptibility testing were performed on clinical samples using the Microscan Walk Away 96 plus system (Beckman Coulter Inc.). Additionally, the presence/absence of carbapenem resistance was determined according to the Clinical and Laboratory Standards Institute’s guidelines. For all patients admitted to the ICU, CHG bathing was conducted once daily in the morning using a cloth impregnated with 2% CHG (Huons Meditech Inc.).

The medical records of patients admitted to the ICU between April 2017 and December 2019 were retrospectively reviewed. During this period, adults aged 18 years and above admitted to the ICU were enrolled while those who stayed in the ICU for less than 2 days were excluded. Patients in whom CRE was isolated by the screening test at the time of admission or from clinical samples obtained within 48 h of admission were also excluded. Patients whose hospital stay spanned the pre- and post-intervention periods were also excluded, as it was not possible to assess the effect of the intervention in such cases.

Baseline characteristics and variables known to be risk factors for CRE acquisition were collated [12] including age, sex, body mass index, comorbidities, Charlson’s comorbidity index, Sequential Organ Failure Assessment (SOFA) score at the time of ICU admission, history of antibiotic administration within 30 days, and receipt of invasive procedures. Invasive procedures included mechanical ventilation, tracheostomy, central venous catheter insertion, feeding tube insertion, urinary catheter insertion, and continuous renal replacement therapy. The duration of ICU stay and in-hospital mortality were also reviewed. The risk of acquiring CRE increases with the number of patients colonised with CRE during hospitalisation. Since this can act as a confounder in CRE acquisition, we defined the colonisation pressure of CRE [13]; this was defined for each patient via a cumulative count of patients colonised with CRE who stayed in the ICU during the same period.

The primary outcome was CRE acquisition, defined as a case in which CRE was identified in the clinical samples or surveillance test performed 48 h after ICU admission but had a negative test result on the initial screening test. CRE acquisition rates before and after the intervention were compared using Kaplan–Meier analysis and the log-rank test; for comparison between the pre- and post-intervention periods, continuous variables were analysed using the Mann–Whitney U test, and categorical variables were analysed using the chi-squared and Fisher's exact tests. The independent risk factors for CRE acquisition were analysed using the multivariable Cox proportional hazard model.

The incidence rates of MDROs including MRSA, VRE, carbapenem-resistant Pseudomonas aeruginosa, and carbapenem-resistant Acinetobacter baumannii in the ICU during the study period were calculated. Additionally, compliance with hand hygiene and adherence to isolation precautions during the study period were evaluated. The temporal change in MDRO incidence, compliance with hand hygiene, and isolation precautions according to year were also analysed using Poisson regression. Statistical analysis was performed using R software (version 4.3.3, R Foundation for Statistical Computing, Vienna, Austria).

The study was approved by the Institutional Review Board of Soonchunhynag Seoul University Hospital (IRB No. 2023-09-017), which waived the need for informed consent owing to the retrospective study design.

Of 1,747 patients who contributed 22,618 patient-days, 35 acquired CRE during their ICU stays. The CRE acquisition rate was 1.94 per 1,000 patient-days during the pre-intervention period and 1.45 per 1,000 patient-days during the post-intervention period. There was no significant difference in the acquisition rate of CRE according to the Kaplan–Meier analysis (log-rank p = 0.357) (Fig. 1). In 2019, the incidence rate of MDRO colonisation decreased from 19.33 per 1,000 patient-days in 2017 to 13.57 per 1,000 patient-days, and Poisson regression analysis revealed a relative risk of 0.85 [95% confidence interval (CI): 0.738–0.945, p = 0.004] (Fig. 2). During the study period, hand hygiene and isolation precaution compliance remained high, exceeding 90% and 80%, respectively, and Poisson regression did not reveal any statistically significant changes over time (Supplementary Figure A1).

Table 1 presents a comparison of baseline characteristics between the pre-intervention and post-intervention groups. In the post-intervention group, the median age and SOFA score were significantly higher at 70 years and 8 points, respectively, compared to the corresponding values of 69 years and 7 points in the pre-intervention group. First-generation cephalosporin exposure was significantly higher in the pre-intervention group at 17.7% compared to 13.5% in the post-intervention group, while carbapenem exposure was significantly higher in the post-intervention group at 27.9% compared to 20.8% in the pre-intervention group. In terms of therapeutic variables, the frequency of central venous catheter insertions was significantly higher in the post-intervention group at 65.5% compared to 56.8% in the pre-intervention group. Lastly, the length of ICU stay and in-hospital mortality did not differ significantly between the two periods.

Table 1

Comparison of baseline characteristics between pre-and post-intervention groups
Variable		Pre-intervention† (n = 451)	Post-intervention (n = 1296)	P-value
Age, years (IQR)		69 (54, 79)	70 (57, 79)	0.027*
Sex, M (%)		253 (56.1%)	727 (56.1%)	1.000
Body mass index (kg/m²) (IQR)		22.4 (19.5, 25.2)	22.2 (19.5, 25.0)	0.661
Charlson’s comorbidity index (IQR)		2 (1, 4)	2 (1,4)	0.135
SOFA score (IQR)		7 (5, 10)	8 (5, 11)	0.023*
Single room occupancy		10 (2.2%)	45 (3.5%)	0.213
Number of CRE colonizers present during ICU stay		3 (2, 3)	2 (1, 3)	0.184
Prior exposure to antibiotics
	Beta-lactam and beta-lactam inhibitor	240 (53.2%)	722 (55.7%)	0.379
	First generation cephalosporin	80 (17.7%)	175 (13.5%)	0.030*
	Second generation cephalosporin	10 (2.2%)	40 (3.1%)	0.414
	Third generation cephalosporin	107 (23.7%)	254 (19.6%)	0.068
	Fourth generation cephalosporin	44 (9.8%)	125 (9.6%)	1.000
	Aminoglycoside	7 (1.6%)	18 (1.4%)	0.819
	Fluoroquinolone	112 (24.8%)	321 (24.8%)	1.000
	Carbapenem	94 (20.8%)	362 (27.9%)	0.003*
	Vancomycin	119 (26.4%)	338 (26.1%)	0.901
Therapeutic variables
	Mechanical ventilation	224 (49.7%)	678 (52.3%)	0.352
	Tracheostomy	55 (12.2%)	202 (15.6%)	0.089
	Central venous catheter	256 (56.8%)	849 (65.5%)	0.001*
	Feeding tube	262 (58.1%)	819 (63.2%)	0.056
	Urinary catheter	395 (87.6%)	1144 (88.3%)	0.736
	Continuous renal replacement therapy	85 (18.8%)	242 (18.7%)	0.944
Duration of hospital stay
	Length of ICU stay (days) (IQR)	6 (4, 11)	7 (4, 14)	0.128
CRE acquisition		9 (2.0%)	26 (2.0%)	1.000
In-hospital mortality		142 (31.5%)	392 (30.2%)	0.635

† The intervention includes universal contact precautions and chlorhexidine gluconate bathing.

*P < 0.05; IQR, interquartile range; M, male; SOFA, Sequential Organ Failure Assessment; ICU, intensive care unit; CRE, carbapenem-resistant Enterobacterales

The multivariable Cox regression model revealed that CRE acquisition was significantly associated with exposure to carbapenem [adjusted hazard ratio (aHR), 2.555; 95%CI: 1.208–5.405; p = 0.014] and the presence of more than four patients colonised with CRE during their ICU stay (aHR, 2.639; 95%CI: 1.226–5.684; p = 0.013). No significant association was observed between UCP and CHG bathing and the acquisition of CRE (aHR, 0.657; 95%CI: 0.301–1.433; p = 0.291) (Table 2).

Table 2

Risk factors for the acquisition of carbapenem-resistant Enterobacterales
Variable	Univariate analysis			Multivariate analysis
Variable	HR	95% CI	P-value	aHR	95% CI	P-value
Age
≤65 years	1
>65 years	1.113	0.544–2.278	0.769
Sex
Male	1
Female	1.035	0.524–2.044	0.922
Charlson’s comorbidity index
≤3	1			1
>3	1.756	0.886–3.482	0.107	1.478	0.729-3.000	0.279
SOFA score
≤6	1
>6	0.623	0.297–1.308	0.211
Carbapenem
Not exposed	1			1
Exposed	2.753	1.332–5.691	0.006	2.555	1.208–5.403	0.014*
Beta-lactam and beta-lactamase inhibitor
Not exposed	1
Exposed	1.031	0.507-2.100	0.932
Third or fourth-generation cephalosporin
Not Exposed	1
Exposed	0.866	0.419	1.789
Vancomycin
Not exposed	1
Exposed	1.209	0.605–2.413	0.591
Fluoroquinolone
Not exposed	1
Exposed	0.830	0.405–1.702	0.612
Mechanical ventilation
Not applied	1
Applied	0.691	0.310–1.542	0.367
Tracheostomy
Not performed	1
Performed	0.912	0.437–1.902	0.805
Central venous catheter
Not applied	1
Applied	1.196	0.518–2.761	0.675
Tube feeding
Not applied	1
Applied	0.875	0.293–2.620	0.812
Urinary catheter
Not applied	1
Applied	0.845	0.297–2.407	0.753
CRRT
Not applied	1			1
Applied	1.610	0.798–3.251	0.184	1.144	0.548–2.389	0.721
Number of CRE colonizers present during ICU stay
≤4	1			1
>4	2.715	1.256–5.869	0.011*	2.639	1.226–5.684	0.013*
Universal contact precautions and CHG bathing
Before intervention	1			1
After intervention	0.696	0.320–1.513	0.360	0.657	0.301–1.433	0.291
*P < 0.05; HR, hazard ratio; aHR, adjusted hazard ratio; CI, confidence interval; SOFA, Sequential Organ Failure Assessment; CRRT, continuous renal replacement therapy; CRE, carbapenem-resistant Enterobacterales; ICU, intensive care unit; CHG, chlorhexidine gluconate.

The findings of this study showed that the rates of CRE acquisition before and after the implementation of UCP and CHG bathing did not differ significantly. Additionally, the intervention was not identified as an independent risk factor for CRE acquisition. However, owing to the very low incidence of CRE acquisition in our study compared to other studies, these results lack generalizability [8, 14]. This study was also underpowered, which hindered the determination of the effect of UCP and CHG bathing on CRE infection. Nonetheless, the results suggest that in regions or hospitals with low CRE incidence, UCP and CHG bathing have limited effects in addition to conventional infection control measures.

If the study’s analysis were to include other MDROs in addition to CRE or be conducted in an area of high CRE prevalence, the effect size and statistical power may have been higher, which may have led to different results [8, 14]. Since we only performed screening tests for CRE at admission, we could not compare the acquisition rates of other MDROs in our study. However, the significant decrease in the incidence rate of other MDROs in the ICU during the study period could be attributed to UCP and CHG bathing.

Compliance of healthcare personnel with UCP and inadequate CHG bathing may have contributed to the findings of our study. Although adherence to isolation precautions in the ICU remained relatively high at over 80% throughout the study period with no significant changes observed over time, evaluation solely by overt observers raises the possibility of overestimation due to the Hawthorne effect [15]. The concentration of CHG on patients’ skin can be monitored using colourimetric assays to assess the appropriateness of CHG bathing. Feedback on the monitoring results can improve the appropriateness of CHG bathing by healthcare personnel [16]. If our study had evaluated and provided feedback on the appropriateness of CHG bathing, it might have increased the effect size of the intervention and affected the significance of the results.

Multivariable Cox regression identified recent exposure to carbapenem within the past 30 days as an independent risk factor for CRE acquisition, which underscores the importance of antibiotic stewardship in reducing the acquisition or transmission of MDROs. Studies on the effect of antimicrobial stewardship programs in reducing the incidence of multidrug-resistant gram-negative bacteria have accumulated substantial evidence [17]. Additionally, CRE colonisation pressure was also identified as an independent risk factor for CRE acquisition, suggesting the possibility that CRE acquisition during the study period occurred due to hospital transmission. This emphasises the importance of standard precautions such as environmental cleaning and hand hygiene.

As contact precautions have been recommended as part of infection control measures, studies have investigated their adverse effects [7, 18, 19]. Contact precautions can reduce the frequency of contact between healthcare workers and patients, and can also diminish patient satisfaction with medical care and lead to various psychological problems such as depression and anxiety. Therefore, it is essential to consider the prevalence of MDROs in the region or hospital, the hospital setting (whether composed mainly of single rooms or multibed bays), and patient factors and weigh the advantages and disadvantages before deciding to implement UCP.

Several studies have identified the effectiveness of CHG bathing in reducing the acquisition of gram-positive organisms, such as MRSA and VRE, as well as decreasing healthcare-associated infections [9, 20, 21]. However, evidence of its effectiveness against gram-negative bacteria remains limited [10, 11]. Our study was underpowered, which limits interpretation; however, we found that the effect size of CHG bathing on CRE acquisition in a low-prevalence area was not substantial. Therefore, it would not be appropriate to introduce CHG bathing solely as an intervention for multidrug-resistant gram-negative bacteria such as CRE in non-endemic areas.

A strength of this study was its large sample size and analysis of the effects of UCP and CHG bathing on CRE acquisition while considering various risk factors for CRE acquisition that could act as confounders. However, several limitations should also be considered. The study was statistically underpowered to detect significant differences in CRE acquisition. Additionally, there is a possibility that temporal changes in variables such as healthcare personnel compliance with infection control measures, which were not considered in the before-and-after design, may have acted as confounders. Furthermore, because both UCP and CHG bathing were implemented simultaneously, it was not possible to separate and analyse the effects of each intervention independently.

The implementation of UCP and CHG bathing did not affect the CRE acquisition rate in the ICU in a low-prevalence area in this study. These interventions should be implemented while considering factors such as the MDRO incidence in the local region, hospital facilities, and the risk to the patient population. A multimodal strategy including antibiotic stewardship should be implemented to control the nosocomial spread of MDROs.

aHR

adjusted hazard ratio

CHG

chlorhexidine gluconate

confidence interval

CRE

carbapenem-resistant Enterobacterales

MDRO

multidrug-resistant organism

MRSA

methicillin-resistant Staphylococcus aureus

ICU

intensive care unit

UCP

universal contact precautions

VRE

vancomycin-resistant Enterococci

Ethics approval and consent to participate

This study was approved by the Institutional Review Board of Soonchunhynag Seoul University Hospital (IRB No. 2023-09-017), which waived the need for informed consent owing to the retrospective study design.

Availability of data and materials

The datasets used and/or analysed during the study are available from the corresponding author upon reasonable request.

Competing interests

The authors declare that they have no competing interests.

Funding

This research was supported by the Soonchunhyang University Research Fund.

Authors' contributions

Conceptualization, Methodology, Writing – original draft, Investigation, Data curation, Formal analysis: J.J, Y.J.B, E.L, T.H.K, Data collection and interpretation: H.P, S.O, J.C, S.A, Y.J, J.K, Writing – review & editing: J.J, Y.J.B, E.L, T.H.K. All authors have provided final approval for the final version of the manuscript.

Acknowledgements

We would like to thank Editage (www.editage.co.kr) for English language editing.

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No competing interests reported.

SupplementaryFigure.tif
Supplementary Figure A1. Compliance with hand hygiene and isolation precautions by healthcare workers according to year HH, hand hygiene; IP, isolation precaution; RR, relative risk; CI, confidence interval

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Impact of universal contact precautions and chlorhexidine bathing on the acquisition of carbapenem-resistant Enterobacterales in the intensive care unit: A cohort study

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