Data concerning intensive care unit (ICU)-acquired bacterial colonization and infections are scarce from low and middle-income countries (LMICs). ICU patients in these settings are at high risk of becoming colonized and infected with antimicrobial-resistant organisms (AROs). We conducted a prospective observational study at the Ho Chi Minh City Hospital for Tropical Diseases, Vietnam from November 2014 to January 2016 to assess the ICU-acquired colonization and infections, focusing on the five major pathogens in our setting: Staphylococcus aureus (S. aureus), Escherichia coli (E. coli), Klebsiella spp., Pseudomonas spp. and Acinetobacter spp., among adult patients with more than 48 hours of ICU stay. We found that 61.3% (223/364) of ICU patients became colonized with AROs: 44.2% (161/364) with rectal ESBL-producing E. coli and Klebsiella spp.; 30.8% (40/130) with endotracheal carbapenemase-producing Acinetobacter spp.; and 14.3% (52/364) with nasal methicillin-resistant S. aureus. The incidence rate of ICU patients becoming colonized with AROs was 9.8 (223/2,276) per 100 patient days. Significant risk factor for AROs colonization was the Charlson Comorbidity Index score. The proportion of ICU patients with HAIs was 23.4% (85/364), and the incidence rate of ICU patients contracting HAIs was 2.3 (85/3,701) per 100 patient days. The vascular catheterization (central venous, arterial and hemofiltration catheter) was significantly associated with hospital-acquired bloodstream infection. Of the 77 patients who developed ICU-acquired infections with one of the five specified bacteria, 44 (57.1%) had prior colonization with the same organism. Vietnamese ICU patients have a high colonization rate with AROs and a high risk of subsequent infections. Future research should focus on monitoring colonization and the development of preventive measures that may halt spread of AROs in ICU settings.
Research Article; Medicine and health sciences; Health care; Health care facilities; Hospitals; Intensive care units; Biology and life sciences; Anatomy; Digestive system; Gastrointestinal tract; Rectum; Infectious diseases; Bacterial diseases; Tetanus; Nosocomial infections; Ecology and environmental sciences; Species colonization; Acinetobacter infections; Organisms; Bacteria; Acinetobacter; Microbiology; Medical microbiology; Microbial pathogens; Bacterial pathogens; Pathology and laboratory medicine; Pathogens; Klebsiella infections
Hospital-acquired infections (HAIs) are a major global health problem, with World Health Organization (WHO) estimating that millions of patients are affected each year [[
Prior bacterial colonization may increase the risk of subsequent HAIs in ICU. Many studies have investigated the relationship between colonization on admission to ICU and subsequent infection. Admission colonization with S. aureus has been shown to be a significant risk factor for ICU-acquired S. aureus infections [[
Understanding colonization and its relationship to HAIs is central for providing the necessary data to ensure safe and high-quality healthcare. In LMICs, such as Vietnam, there is a large amount of antimicrobial use in the community [[
We conducted a prospective observational study in Adult ICU of the Ho Chi Minh City Hospital for Tropical Diseases, a tertiary referral hospital for infectious diseases serving Southern Vietnam. Adult ICU is a 20-bed medical ward, but usually admits additional patients. There are approximately 24–28 patients per day and 1,000–1,200 admissions per year. The nurse-to-patient ratio is about 1:3, and varying numbers of nursing students may also be present and take part in clinical activities. The ICU is divided into 4 small blocks (about 4–8 patients per block). The standard infection control measures are in place, including personal protective equipment for routine patient care (head coverings, mask, and gloves); daily patient bathing with 2% chlorhexidine gluconate; healthcare worker education and adherence monitoring with a focus on hand hygiene. The mean rate of hand hygiene compliance in Adult ICU is about 70–80%. Anios Special DJP SF (Laboratoires Anios
The study was reviewed and approved by the Ethics Committee of the Ho Chi Minh City Hospital for Tropical Diseases, Vietnam and the Oxford Tropical Research Ethics Committee (OxTREC), United Kingdom.
All patients aged ≥15 years admitted to ICU with an expected length of stay of >48 hours between 10th November 2014 and 14th January 2016 were eligible for entry to the study. Written informed consent was obtained from all the participants or their representatives. All patients admitted to ICU within 90 days from an earlier discharge were excluded. Nasal swab, rectal swab, and/or endotracheal aspirate (in case of intubation or tracheostomy) were taken for detecting acquired colonization with S. aureus, E. coli, Klebsiella spp., Acinetobacter spp. and Pseudomonas spp. and subsequent HAIs. Swabs were taken within 48 hours of ICU admission and repeated twice a week (on Monday and Thursday) until patients were discharged from ICU.
Nasal and endotracheal specimens were cultured on Blood agar (bioMérieux) and MacConkey (bioMérieux) to specifically isolate S. aureus, E. coli, Klebsiella spp., Pseudomonas spp. and Acinetobacter spp.. Staphylococcal colonies were checked for catalase and coagulase, plus checked for methicillin resistance using cefoxitin disc diffusion, and re-checked on the matrix assisted laser desorption/ionization time-of-flight mass spectrometry (MALDITOF, Bruker) [[
Xylose Lysine Deoxycholate agar (bioMérieux) and MacConkey agar (bioMérieux) were used to culture rectal swabs for Gram negative bacteria, and identification of E. coli, Klebsiella spp., Pseudomonas spp. and Acinetobacter spp. was confirmed by MALDITOF. Antimicrobial susceptibility testing was conducted by the Kirby/Bauer disc diffusion method and interpreted using the Clinical and Laboratory Standards Institute guidelines 2015 [[
Other clinical specimens (blood, urine and sputum) were cultured according to the Standard Operating Procedure of the Microbiology Department of the Ho Chi Minh City Hospital for Tropical Diseases.
For the purposes of this investigation, acquired colonization was defined by a positive surveillance culture with S. aureus, E. coli, Klebsiella spp., Pseudomonas spp. and/or Acinetobacter spp. preceded by a negative culture on admission or a positive surveillance culture with differently specified bacteria or with the same organisms but different resistance pattern compared to admission culture. Antimicrobial-resistant organisms (AROs) colonization was defined as a positive culture from nasal, rectal and/or endotracheal sample of methicillin-resistant S. aureus, 3
Risk factors for specifically acquired nasal/rectal/endotracheal colonization with AROs during ICU stay were evaluated using Cox proportional cause-specific hazards regression, with discharge and death as competing events. The following possible risk factors on ICU admission were investigated: tetanus disease, Charlson Comorbidity Index score, colonization status (by anatomical sites), receipt of antimicrobial treatment, and intensive care procedures including nasogastric tube and respiratory support consisting of intubation, tracheostomy and mechanical ventilation. Respiratory support was tested for nasal and endotracheal (not for rectal) colonization with AROs. Tetanus disease was included in the model because the pathogenesis of tetanus disease is related to the activity of a neuro-toxin released from Clostridium tetani [[
Cox proportional hazards regression was also used to determine the risk factors for specific types of HAIs: pneumonia, BSI and UTI, and only the first episode of HAIs caused by any of the specified bacteria was included for analysis. However, multivariate Cox regression model was not performed for BSI due to a very low number of events. The following risk factors were considered: admission for tetanus disease, Charlson Comorbidity Index score, prior colonization status (including initial colonization on ICU admission and acquired colonization during ICU stay per anatomical sites), and intensive care procedures (respiratory support consisting of intubation, tracheostomy and mechanical ventilation for pneumonia; urinary catheter for UTI; and vascular catheters including central venous, arterial and hemofiltration catheter for BSI). In this model, prior nasal/rectal/endotracheal colonization is considered as a time-dependent risk factor in subsequent HAIs. Time zero was the date of ICU admission, and the date of acquired colonization was assumed to be at the midway point between the latest negative culture and the first positive surveillance culture. It was assumed that patients remained colonized from detection of colonization on ICU admission or acquisition during ICU stay until ICU discharge.
Statistical analyses used the R 3.4.0 software (R foundation, Vienna, Austria), especially the R functions coxph from the survival package. P values < 0.05 (two-sided) were considered statistically significant.
838 adults were enrolled in the study, of whom 364 were admitted for >48 hours and were screened for acquired colonization and HAIs (Fig 1). Of note is the large proportion of patients in this study with tetanus (56.0%, 204/364). The patient characteristics are described in Table 1.
Table 1: General patient characteristics during ICU stay.
Age (yr)–median (IQR) 46 (33–60) < 60 –n (%) 265 (72.8) ≥ 60 –n (%) 99 (27.2) Sex–n (%) Male 242 (66.5) Female 122 (33.5) Charlson Comorbidity Index score–median (IQR) 0 (0–1) No comorbidity (0)–n (%) 247 (67.8) Mild (1–2)–n (%) 73 (20.1) Moderate (3–4)–n (%) 24 (6.6) Severe (≥ 5)–n (%) 20 (5.5) APACHE II score–median (IQR) 8 (3–14) Mild (< 5)–n (%) 118 (32.4) Moderate (5–12)–n (%) 134 (36.8) Severe (> 12)–n (%) 112 (30.8) Admitting diagnosis–n (%) Tetanus 204 (56.0) Sepsis and septic shock 75 (20.6) Local infections* 45 (12.4) Dengue infection 17 (4.7) Internal medicine diseases# 23 (6.3) Death–n (%) 40 (11.0) ICU stay (days)–median (IQR) 10 (5–18) Hospital stay (days)–median (IQR) 22 (13–32)
1 * Local infections included pneumonia (25 cases), cellulitis (4 cases), UTI (15 cases), and spontaneous bacterial peritonitis (1 cases)
2 # Internal medicine diseases included kidney failure (6 cases), myocarditis (3 cases), myocardial infarction (6 cases), atrial fibrillation (3 cases), malignant hypertension (2 cases), diabetic ketoacidosis (2 cases) and epilepsy (2 cases).
In this study, a total of 3,162 surveillance swabs were taken: 1,276 nasal swabs, 1,276 rectal swabs, and 610 endotracheal samples from 130 patients with endotracheal tubes in place. A total of 3,836 bacterial isolates were cultured, of which 378 (9.9%) were S. aureus, 1,550 (40.4%) were E. coli, 895 (23.3%) were Klebsiella spp., 555 (14.5%) were Acinetobacter spp., and 458 (11.9%) were Pseudomonas spp.. Their antimicrobial resistance characteristics are summarized in Table 2.
Table 2: Antimicrobial resistance of colonized bacteria (in percentage).
Antimicrobialsn (%) S.aureus (n = 378) E.coli (n = 1,550) Klebsiella spp. (n = 895) Acinetobacter spp. (n = 555) Pseudomonas spp. (n = 458) Amoxcillin-clavulanic acid 924 (59.6) 260 (29.1) Ceftazidime 881 (56.8) 256 (28.6) 539 (97.1) 101 (22.1) Ceftriaxone 881 (56.8) 256 (28.6) 539 (97.1) Cefepime 811 (52.3) 213 (23.8) 539 (97.1) 87 (19.0) Ticarcillin-clavulanate 984 (63.5) 277 (30.9) 537 (96.8) 330 (72.1) Piperacillin-tazobactam 815 (52.6) 219 (24.5) 537 (96.8) 81 (17.7) Ofloxacin 767 (49.5) 131 (14.6) Ciprofloxacin 227 (60.1) 780 (50.3) 183 (20.4) Levofloxacin 221 (58.5) 352 (63.4) 56 (12.2) Sulfamethoxazole-trimethoprim 19 (5.0) 1,102 (71.1) 335 (37.4) 302 (54.4) 438 (95.6) Amikacin 25 (1.6) 27 (3.0) 215 (38.7) 23 (5.0) Gentamycin 23 (5.0) Ertapenem 42 (2.7) 32 (3.6) Imipenem 33 (2.1) 32 (3.6) 371 (66.8) 202 (44.1) Meropenem 26 (1.7) 32 (3.6) 371 (66.8) 183 (40.0) Colistin 27 (1.7) 44 (4.9) 6 (1.1) 0 Penicillin 368 (97.4) Oxacillin 275 (72.8) Vancomycin 0 Erythromycin 265 (70.1) Rifampicin 30 (7.9) Clindamycin 269 (71.1)
The proportion of patients who acquired either nasal, rectal and/or endotracheal colonization with an ARO was 61.3% (223/364, Fig 2). The 364 patients included in the study represented a total of 2,276 patient days at risk of AROs acquisition in ICU. Therefore, the incidence rate of ICU patients becoming colonized with AROs was 9.8 (223/2,276) per 100 patient days. The acquired AROs colonization rate of the tracheal tract was the highest (61.5%, 80/130), followed by the rectal colonization (54.7%, 199/364) and the nasal colonization (33.8%, 123/364). The overall acquisition risk at any sampling site with an ESBL-producing E. coli was 39.8% (145/364), carbapenemase-producing Acinetobacter spp. 22.0% (80/364), methicillin-resistant S. aureus 16.2% (59/364), ESBL-producing Klebsiella spp. 13.7% (50/364), carbapenemase-producing Pseudomonas spp. 11.8% (43/364), carbapenemase-producing E. coli 3.3% (12/364) and carbapenemase-producing Klebsiella spp. 3.3% (12/364). Carbapenem-resistant Acinetobacter spp. and methicillin-resistant S. aureus were the most commonly isolated organisms from nasal swabs, cultured from 15.7% (57/364) and 14.3% (52/364) of patients, respectively. These two organisms were also the most commonly isolated organisms from endotracheal aspirates 30.8% (40/130) and 26.9%, (35/130), respectively. The rate of rectal colonization with 3
In our univariate analysis (Table 3), we found Charlson Comorbidity Index score as a significant risk factor for acquired colonization with AROs, regardless of anatomical sites (all p-values ≤ 0.01), while receipt of antimicrobial treatment on ICU admission was a significant risk factor for nasal and rectal colonization with AROs (both p-values ≤ 0.001). Admission for tetanus disease reduced the risk of AROs acquisition in nasal and rectal cavity (both p-values ≤ 0.001), and nasogastric tube was associated with reduced risk of rectal AROs colonization (p = 0.01).
Table 3: Univariate hazard ratios for risk factors for acquired colonization with AROs, according to Cox regression analysis.
Variables Nasal colonization (N = 123) Rectal colonization (N = 199) Endotracheal colonization (N = 80) HR (95% CI) p HR (95% CI) p HR (95% CI) p Admission for tetanus disease 0.40 (0.27–0.60) <0.001 0.37 (0.27–0.51) <0.001 0.63 (0.35–1.13) 0.12 Charlson Comorbidity Index score 1.25 (1.08–1.44) 0.003 1.24 (1.12–1.37) <0.001 1.45 (1.09–1.93) 0.01 Admission colonization status Admission nasal colonization 0.65 (0.37–1.12) 0.12 - - - - Admission rectal colonization - - 1.12 (0.76–1.64) 0.57 - - Admission endotracheal colonization - - - - 0.86 (0.47–1.57) 0.63 Receipt of antimicrobial treatment on admission 1.96 (1.31–2.95) 0.001 1.89 (1.38–2.59) <0.001 1.44 (0.83–2.51) 0.19 Intensive care procedures on admission Nasogastric tube 1.14 (0.79–1.66) 0.48 0.69 (0.51–0.92) 0.01 0.83 (0.52–1.32) 0.42 Respiratory support 1.34 (0.93–1.92) 0.11 - - 0.91 (0.58–1.43) 0.69
In multivariate analysis (Table 4), hazard ratios did not change much, except for antimicrobial treatment, which was reduced by at least 50% and became non-significant, and Charlson Comorbidity Index score, which was reduced and was no longer a significant risk factor for nasal colonization with AROs. Still, admission for tetanus disease had reduced the risk of nasal and rectal acquisition by AROs, while nasogastric tube reduced the incidence of rectal AROs colonization in ICU.
Table 4: Multivariate hazard ratios for risk factors for acquired colonization with AROs, according to Cox regression analysis.
Variables Nasal colonization (N = 123) Rectal colonization (N = 199) Endotracheal colonization (N = 80) HR (95% CI) p HR (95% CI) p HR (95% CI) p Admission for tetanus disease 0.46 (0.29–0.74) 0.001 0.39 (0.27–0.56) <0.001 0.67 (0.33–1.36) 0.27 Charlson Comorbidity Index score 1.14 (0.97–1.35) 0.12 1.13 (1.01–1.25) 0.04 1.42 (1.03–1.94) 0.03 Admission colonization status Admission nasal colonization 0.57 (0.32–1.01) 0.05 - - - - Admission rectal colonization - - 1.19 (0.80–1.76) 0.40 - - Admission endotracheal colonization - - - - 0.76 (0.40–1.45) 0.41 Receipt of antimicrobial treatment on admission 1.28 (0.80–2.04) 0.31 1.19 (0.84–1.71) 0.33 1.20 (0.66–2.18) 0.55 Intensive care procedures on admission Nasogastric tube 1.05 (0.68–1.61) 0.83 0.62 (0.46–0.83) 0.002 0.80 (0.48–1.33) 0.40 Respiratory support 1.16 (0.77–1.75) 0.49 - - 0.82 (0.50–1.35) 0.45
During the study period, 106 episodes of HAIs were observed in 85 patients, of whom 66 patients (77.6%) had a single episode, 18 (21.2%) had two episodes, and 1 (1.2%) had four episodes. The 364 patients included in the study represented a total of 3,701 patient days at risk of contracting HAIs in ICU. Therefore, the proportion of ICU patients with HAIs was 23.4% (85/364), and the incidence rate of ICU patients contracting HAIs was 2.3 (85/3,701) per 100 patients days. The most common type of HAIs were pneumonia (49.1%, 52/106), of which 69.2% (36/52) were ventilator associated infections, followed by urinary tract infections (36.8%, 39/106) and bloodstream infections (14.1%, 15/106). The mean time from admission to the first episode of HAIs was 11.9 ± 6.4 days. Of the 106 episodes of HAIs, 93 (87.7%) were linked to the culture of a single bacterial species and 13 (14.0% of 93) were associated with more than one organism. The distribution of pathogens causing HAIs is shown in Fig 3.
Table 5 shows the relationship between bacterial species of HAIs and prior colonization (either admission colonization or acquired colonization). For example, 100% of the 15 patients with subsequent sensitive Klebsiella spp. infections had prior antimicrobial susceptible Klebsiella spp. isolated from nasal swabs, rectal swabs and/or endotracheal aspirates. Among the 14 patients who developed carbapenemase-producing Acinetobacter spp. infections, 7 (50.0%) had prior colonization with carbapenemase-producing Acinetobacter spp.; 6 (66.7%) of the 9 patients with methicillin-resistant S. aureus infections had prior methicillin-resistant S. aureus colonization.
Table 5: Subsequent hospital-acquired infections and prior colonization (either admission colonization or acquired colonization) with the same organisms among ICU patients.
Bacteria Hospital-acquired infections (n) Prior colonization (n, %) Yes No Sensitive S. aureus 5 2 (40.0%) 3 (60.0%) Methicillin-resistant S. aureus 9 6 (66.7%) 3 (33.3%) Sensitive E. coli 3 3 (100%) 0 ESBL-producing E. coli 8 6 (75.0%) 2 (25.0%) AmpC-producing E. coli 3 0 3 (100%) Sensitive Klebsiella spp. 15 15 (100%) 0 ESBL-producing Klebsiella spp. 1 1 (100%) 0 AmpC-producing Klebsiella spp. 1 1 (100%) 0 Carbapenemase-producing Klebsiella spp. 1 0 1 (100%) Sensitive Acinetobacter spp. 2 1 (50.0%) 1 (50.0%) ESBL-producing Acinetobacter spp. 4 1 (25.0%) 3 (75.0%) Carbapenemase-producing Acinetobacter spp. 14 7 (50.0%) 7 (50.0%) Sensitive Pseudomonas spp. 9 1 (11.1%) 8 (88.9%) Carbapenemase-producing Pseudomonas spp. 2 0 2 (100%) Total 77 44 (57.1%) 33 (42.9%)
In univariate analysis (Table 6), vascular catheters including central venous, arterial and hemofiltration catheter were found to be a significant risk factor for hospital-acquired bloodstream infection (p = 0.01). Both univariate and multivariate Cox regression analysis (Tables 6 and 7) demonstrated that admission for tetanus disease was a protective factor against the development of hospital-acquired pneumonia in ICU, whereas none of the study factors was significantly associated with HAIs.
Table 6: Univariate hazard ratios for risk factors of hospital-acquired infections, according to Cox regression analysis.
Variables Pneumonia (N = 44) Urinary tract infection (N = 38) Bloodstream infection (N = 15) HR (95% CI) p HR (95% CI) p HR (95% CI) p Admission for tetanus disease 0.31 (0.16–0.62) 0.001 1.38 (0.52–5.13) 0.55 0.34 (0.12–1.08) 0.07 Charlson Comorbidity Index score 1.28 (0.92–1.62) 0.13 0.87 (0.37–1.41) 0.66 1.31 (0.86–1.74) 0.17 Prior colonization status Prior nasal colonization 0.51 (0.22–1.33) 0.16 - - - - Prior rectal colonization - - 0.49 (0.06–63.59) 0.66 0.52 (0.06–68.40) 0.69 Prior endotracheal colonization 0.77 (0.40–1.55) 0.45 - - - - Intensive care procedures on admission Urinary catheter - - 0.83 (0.41–1.64) 0.60 - - Respiratory support 1.30 (0.71–2.38) 0.39 - - - - Vascular catheters - - - - 5.06 (1.45–15.22) 0.01
Table 7: Multivariate hazard ratios for risk factors of hospital-acquired infections, according to Cox regression analysis.
Variables Pneumonia (N = 44) Urinary tract infection (N = 38) HR (95% CI) p HR (95% CI) p Admission for tetanus disease 0.33 (0.16–0.67) 0.002 1.25 (0.41–4.88) 0.72 Charlson Comorbidity Index score 1.04 (0.71–1.53) 0.84 0.93 (0.39–1.47) 0.82 Prior colonization status Prior nasal colonization 0.47 (0.16–1.37) 0.17 - - Prior rectal colonization - - 0.50 (0.06–64.94) 0.67 Prior endotracheal colonization 0.84 (0.37–1.90) 0.69 - - Intensive care procedures on admission Urinary catheter - - 0.85 (0.41–1.68) 0.64 Respiratory support 1.28 (0.65–2.55) 0.48 - - Vascular catheters - - - -
Reports on ICU-acquired bacterial colonization are well-described in high-income settings. To our knowledge, our study is the first prospective longitudinal study to investigate ICU-acquired colonization in Vietnam and one of the few investigating this in a LMIC setting. Our findings show that Vietnam has a high rate of ICU-acquired colonization with AROs (61.3%), especially with methicillin-resistant S. aureus (16.2%) and ESBL-producing Enterobacteriaceae (including 39.8% for E. coli and 13.7% for Klebsiella spp.). The reason behind is multifactorial, but maybe associated with a high proportion of study patients (38.2%) were treated with broad-spectrum antimicrobials within 48 hours of ICU admission which had a negative impact on surveillance culture of all samples. Therefore, more sensitive organisms may not have been detected, resulting in favor of more resistant ones. Moreover, contact isolation or geographic separation of colonized or infected patients with AROs is rarely applied in our unit, so this can contribute to the spread of AROs among ICU patients. Our data can be compared to those from China and France where acquired colonization rates with AROs of 15.2–34.4% have been reported in multicenter studies [[
In terms of HAIs, we found that vascular catheters including central venous, arterial and hemofiltration catheter were the main risk factor for hospital-acquired BSI. This is in accordance with other published data showing vascular catheterization increases the risk of infection because of damaging human natural barriers against infection like skin or mucous membranes. Moreover, contaminated objects or substances may be introduced directly into tissues [[
Focusing on early identification of risk factors of acquired AROs colonization may aid in reducing the spread of AROs and subsequent HAIs in ICU settings. Here, Charlson Comorbidity Index score was a significant risk factor for rectal and endotracheal colonization of AROs, and it also seems to increase the risk of nasal colonization with AROs in ICU (HR = 1.14, p = 0.12, Table 4). This is in agreement with some studies conducted in other regions of the world [[
Our study is limited by being conducted in a single tertiary center, which limits generalization of its results to other centers. Many environmental factors, like workload, hand hygiene compliance, room cleaning protocols, and patient-related factors were not evaluated for the risk of acquired colonization and infections. Moreover, we did not investigate the genetic mechanisms of antimicrobial resistance to better understand current resistance and evaluate potential interventions.
ICU patients are at high risk for acquiring colonization and contracting HAIs, especially with AROs during ICU stay. Although the results show only benefit in a single center, they offer insight for future research which should focus on monitoring colonization, and the development of preventive measures that may halt spread of AROs in ICU settings.
We would like to thank all doctors, nurses and nursing aids of the Adult ICU of the Ho Chi Minh City Hospital for Tropical Diseases for data assistance, all staffs working in Microbiology Group of OUCRU—Vietnam for laboratory support, and Mr Bui Thanh Lich for building CliRes Data Management System.
DIAGRAM: Fig 1: Inclusion of patients, taking surveillance swabs, and outcomes.
DIAGRAM: Fig 2: Number of patients became colonized during ICU stay. ICU patients became colonized with sensitive organisms are represented by the black color, and those with AROs are shown by the grey color.
DIAGRAM: Fig 3: Number of isolates causing hospital-acquired infections. Sensitive pathogens are represented by the black color. AROs are shown by the grey color.
By Duong Bich Thuy, Writing – original draft; James Campbell, Resources; Le Thanh Hoang Nhat, Methodology; Nguyen Van Minh Hoang, Resources; Nguyen Van Hao, Project administration; Stephen Baker, Writing – review & editing; Ronald B. Geskus, Methodology; Guy E. Thwaites, Writing – review & editing; Nguyen Van Vinh Chau, Supervision and C. Louise Thwaites, Writing – review & editing