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/lp/springer-journals/faucet-aerators-as-a-reservoir-for-carbapenem-resistant-acinetobacter-iqb0deEV70
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- Springer Journals
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- Copyright © 2019 by The Author(s).
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- Biomedicine; Medical Microbiology; Drug Resistance; Infectious Diseases
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- 2047-2994
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- 10.1186/s13756-019-0635-y
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Abstract
Background: On January 7, 2019, we observed an outbreak of healthcare-associated infection (HAI) caused by Carbapenem-resistant Acinetobacter baumannii (CRAB) in the neurosurgical intensive care unit (NSICU). A follow-up epidemiological investigation was conducted, and an emergency response was initiated. We aimed to study the clonal transmission of CRAB and its possible source. Methods: A matched case-control (1:2) study was performed to identify the possible predisposing factors. A multifaceted intervention was implemented to control the outbreak. We collected environmental samples from patients’ rooms and living area of the staff. CRAB isolates were tested for genetic relatedness by Pulsed-Field Gel Electrophoresis (PFGE). Results: Environmental sampling showed that a faucet aerator was contaminated with A. baumannii. Molecular typing revealed the only outbreak strain, which was isolated from tracheal aspirate cultures of the first case of community-acquired infection and 3 cases of HAI. In environmental samples, the outbreak strain was found only in the faucet aerator of the dining room. This CRAB outbreak was discovered in time, and further progress of this outbreak was prevented through a pre-set emergency response procedure. Conclusions: The faucet aerator acted as a reservoir for bacteria in the outbreak, and contamination of the faucet aerator might have occurred from splashes originating from handwashing by the healthcare workers (HCWs). In high-risk areas, such as NSICU, the faucet aerators should not be used during an outbreak or they should be regularly cleaned and disinfected. The start-up criteria for the emergency response played a key role in controlling the CRAB outbreak, and its settings should be discussed more widely. Keywords: Healthcare-associated infection, Outbreak, Acinetobacter baumannii, Emergency response, Neurosurgical intensive care unit, Faucet aerator. * Correspondence: sichuangankongzhou@163.com; 1135531579@qq.com Qian Xiang and Ying Z. Jin contributed equally to this work. Healthcare-associated Infections Control Center, Sichuan Academy of Medical Sciences and Sichuan People’s Hospital, Chengdu, Sichuan, People’s Republic of China Department of Nursing, Jianyang People’s Hospital, Jianyang, Sichuan, People’s Republic of China Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Lv et al. Antimicrobial Resistance and Infection Control (2019) 8:205 Page 2 of 9 Introduction contaminated tap water in ICUs [7–9]. Legionella, S. Carbapenem-resistant Acinetobacter baumannii (CRAB) is maltophilia and Pseudomonas aeruginosa are the most emerging as a problematic pathogen for patients, clinicians, commonly found pathogens in these studies, and rela- and infection-control personnel, owing to high mortality, tively few cases of HAI outbreaks caused by A. bauman- less treatment options, and its ability to contaminate and nii (AB) have been reported. persist in the healthcare environment at high levels [1]. In The faucet aerator played a key role in the tap water the first ever list of the deadliest superbugs that threaten pollution process in previous outbreak cases [10, 11]. In human health published by the World Health Organization an outbreak investigation in Taiwan, Wang found that (WHO) in 2017, CRAB was listed in the “critical” section one-third of the ICU faucet aerators sampled were con- [2]. According to data from the China Antimicrobial Sur- taminated with NFGNB [12]. Verweij inferred that the veillance Network (CHINET), the detection rate of CRAB contaminated aerator screens of tap water outlets were has increased rapidly in the last 10 years. By 2017, about the source of contamination after an investigation of the 66.7 and 69.3% of A. baumannii strains were resistant to outbreak caused by S. maltophilia [13]. imipenem and meropenem [3]. A multi-center study in From December 2018 to January 2019, 7 patients had China showed that the incidence density of all CRAB iso- CRAB positive cultures isolated from the lower respiratory lates was 2.47 per 1000 inpatient-days in the intensive care tract in the neurosurgical ICU (NSICU) of the largest ter- unit (ICU), which was significantly higher than that previ- tiary A-level hospital in Sichuan Province, China. All clin- ously reported in other regions [4, 5]. Theprevalenceof ical isolates were resistant to carbapenems, and their CRAB in China is at high levels, and CRAB has been in- antibiotic-susceptibility patterns were identical. Three of creasingly reported as a cause of nosocomial outbreaks in these 7 patients developed lower respiratory tract infection ICUs [6]. due to CRAB, and they had similar symptoms and signs. A lot of epidemiological and molecular evidence This NSICU was remodeled from a previous rehabilitation suggests that there is a close correlation between ward, and it consisted of two 6-bedded rooms, two 3- healthcare-associated infection (HAI) outbreaks caused bedded rooms, one 2-bedded room, and one isolation by nonfermentative gram-negative bacilli (NFGNB) and room. A map of the NSICU is shown in Fig. 1. Herein, we Fig. 1 Schematic map of NSICU. The symbol in the figure indicates the locations of samples that were positive for CRAB. (●) Patients with isolates positive for CRAB. (▲) Environmental samples positive for CRAB. (〇) Environmental samples from sinks negative for CRAB Lv et al. Antimicrobial Resistance and Infection Control (2019) 8:205 Page 3 of 9 describe a follow-up epidemiological investigation that in- established a hand hygiene compliance monitoring team. cluded environmental sampling and genotyping by Pulsed- After unified training, the team members used the Field Gel Electrophoresis (PFGE). WHO hand hygiene tools to measure monthly hand hy- giene compliance in 92 wards of the hospital. To avoid Materials and methods observation bias, the observation unit was temporarily Epidemiological investigation randomly assigned to each team member. During the The tools provided in the “Guideline for control of an outbreak, daily hand hygiene compliance supervision healthcare-associated infection outbreak (WS/T 524-2016)” was performed by the NSICU head nurse using the same were used for epidemiological investigation [14]. An out- method. break emergency start-up procedure was implemented to detect and contain the HAI outbreak. Case-control study Emergency response criteria for a HAI outbreak were A matched case-control study was performed to verify as follows: the suspicious factors leading to the HAI outbreak. The Since the detection rate of a certain pathogenic micro- cases of HAI were defined as those who had stayed in organism in clinical specimens from a certain depart- the ICU for at least 48 h with CRAB infection or ment has significantly increased, all the past cases within colonization, but it did not include cases of CRAB con- 7 calendar days of the department are reviewed from the tamination and community infections. date of specimen submission, and the emergency re- Controls were patients who met the matching criteria. sponse is initiated if the following conditions are met: For each case patient, 2 control patients were randomly se- lected from the group of patients admitted to the NSICU ① Within 7 calendar days, there were 2 cases or more during the same period who did not acquire CRAB. of HAI or suspected cases of HAI caused by the same Matching criteria were as follows: pathogenic microorganisms with highly similar antibiotic-susceptibility patterns; ① Patients with the same gender and in the same age ② Within 3 calendar days, there were 3 cases or more group as the cases, and the age difference should be of hospital-acquired cases (including colonization, HAI, within 5 years; and suspected HAI) caused by the same pathogenic ② To avoid “time bias,” the selected controls should microorganisms with highly similar antibiotic- have sufficient length of hospitalization stay [17, 18]. susceptibility patterns; Therefore, controls were patients who had been in the NSICU for an interval at least as long as that between With reference to the definition of Repeat Infection the time of NSICU admission and isolation of CRAB Timeframe (RIT) for HAI surveillance by the US National for the case patient; Healthcare Safety Network (NHSN) [15], we determined ③ The Glasgow Coma Scale (GCS) of the controls the following exclusion criteria: should be in the same category as the cases, and the GCS difference should be within 2 scales. The GCS has ① Cases that were judged to be contaminated by the a well-established profile for use in people who have pathogenic microorganisms or were taken outside the sustained a traumatic brain injury, designating them department; into three severity categories; mild (GCS 13–15), ② Patients whose infection had been cured; moderate (9–12), and severe (3–8) categories [19]. ③ Patients who had been hospitalized for a long time (excluding patients who had been hospitalized for more Study sample than 14 days after infection, but did not include new Both clinical and environmental specimens were proc- infections that have been identified), thereby avoiding essed using standard techniques and reagents. Environ- frequent triggering of an emergency response by these mental sampling was performed after cleaning the entire patients. unit. Environmental specimens were collected from sus- pected potential pollutants, including bed rails, door The outbreak period was defined from December 28, handles, curtains, computer keyboards and mice, ventila- 2018 to January 19, 2019. HAIs were defined according tor control panel and sensor, air vents, mattresses, treat- to the “HAI Diagnostic Criteria” issued by the Ministry ment carts, equipment tower surfaces, used rag and of Health of the People’s Republic of China in 2001 [16]. towel, staff hands, used medical textiles, sink inner sur- face, potable water, aerators, the outer surface of the fau- Hand hygiene compliance observation cets, and the inner surface of the proximal end of the Since January 2016, the HAI management department water outlet. The entire exterior of aerators was sampled and the nursing department of our hospital have jointly after dismantling. Pre-moistened cotton swabs were used Lv et al. Antimicrobial Resistance and Infection Control (2019) 8:205 Page 4 of 9 to sample environmental specimens. The swabs were Results immediately inoculated onto sheep blood agar plates Outbreak investigation and response and incubated at 37 °C for 2 to 4 days. On January 7, 2019, the Infection Control Department was notified that the tracheal aspirate culture results of 5 patients in the NSICU showed CRAB positivity. Of these Microbiological methods 5 patients, 1 had CRAB infection before admission, 2 had The standard paper diffusion method and Vitek-2 (BioMer- CRAB HAI, and 2 had CRAB colonization. This state sat- ieux, France) automatic instrument detection was used to isfied our pre-established emergency response criteria for detect the sensitivity of AB to 21 commonly used antibiotics, HAI outbreaks, and therefore, following the emergency including imipenem, meropenem, doripenem, ticarcillin, response process, an outbreak control team was estab- ampicillin/sulbactam, ceftriaxone, cefotaxime, cefepime, lished including an infection control officer, bacteriolo- cefotetan, cefuroxime, cefoperazone/sulbactam, piperacillin/ gists, cleaning staff, NSICU doctors, and nurses. Intensive sulbactam, gentamicin, tobramycin, ciprofloxacin, amikacin, infection control measures and environmental microbial tetracycline, tigecycline, minocycline, amoxicillin/clavulanic sampling were implemented immediately, but their effects acid, and aztreonam. Molecular typing was performed by were poor. Three days after the emergency response, a the CHEF-Mapper PFGE system, and PFGE pattern cluster- new case of infection and a case of colonization occurred. ing analysis was conducted by using BioNumerics Version However, after the use of all faucet aerators in the NSICU 6.64. The PFGE classification was judged according to the was prohibited on January 13, 2019, there were no new discriminant proposed by Tenover et al. [20]. Differences of cases of infection or colonization, other than repeated de- more than 3 bands were considered to be of different types. tection in previous patients, until March 24, 2019, when CRAB was identified in a patient’sairway aspirate speci- men. The timeline of the outbreak investigation is illus- Infection control interventions trated in Fig. 2. Intensive infection control measures were implemented according to the guideline (WS/T 524–2016) during the Isolation of CRAB early outbreak (January 8–12, 2019). They included the All lower respiratory tract samples were obtained from following: (1) Strengthening measures to improve hand tracheal aspirates. Within 3 days from the initiation of hygiene compliance were implemented. Healthcare the emergency response on January 7, 2019, 200 envir- workers’ (HCWs) hand hygiene compliance was checked onmental samples were collected. Only one sample, twice daily, and violators were financially penalized. (2) which was obtained from the faucet aerator in the dining Isolation was strictly enforced. Colonized/infected pa- room, was found to be culture positive. The photograph tients were separated into concentrated areas. (3) Fluor- of the faucet aerator is shown in Fig. 3. All detected AB escent labeling was used to control the daily cleaning were only sensitive to tigecycline and resistant to other and disinfection effect of the ICU environment surface. antibiotics. (4) Aerosolized hydrogen peroxide was used to carry out terminal disinfection of individual wards in turn. (5) Un- Case–control study necessary transfer of patients from other units or sur- Of the 6 cases, 3 scored 4 points on the GCS, 2 scored 5 rounding hospitals was stopped. (6) Contact precautions points on the GCS, and 1 scored 9 points on the GCS. were practiced for all patients. (7) Medical staff and The mean age (±SD) of cases was 70.50 ± 7.31 years. Six cleaning staff were retrained for an emergency response (50%) were men. Three patients (50%) had lower respira- to the HAI outbreak. tory tract infection due to CRAB, and the remaining 3 From January 13, 2019, the use of all faucet aerators in patients had only CRAB colonization of the lower re- the NSICU was prohibited. To avoid the infection risk of spiratory tract. A comparison of the possible risk factors water-borne bacterial contamination due to splashing for CRAB acquisition in cases and controls is shown in after the outbreak, all aerators were immersed once a Table 1. On univariate analysis or by using the multi- week with chlorine disinfectant. variate model, cases and controls did not differ signifi- cantly with respect to the studied characteristics. Statistical methods Molecular typing of CRAB Statistical analysis of the data was performed using SPSS We analyzed molecular typing of 5 strains, including 1 23.0 software. A conditional logistic regression model strain isolated from the faucet aerator in the dining for matched case-control groups was used to identify the room, 1 strain isolated from the clinical samples of the factors associated with CRAB colonization and infection. first case that was infected before admission, and 3 All tests were 2-sided with an level of 0.05. strains isolated from the clinical samples of patients with Lv et al. Antimicrobial Resistance and Infection Control (2019) 8:205 Page 5 of 9 Fig. 2 Progress of the CRAB outbreak in the NSICU. The solid line indicates the patients’ hospitalization status in the NSICU. The blue solid bar indicates that the patient is in CRAB HAI status. The wavy texture bar indicates that the patient is in CRAB colonization status. The Vertical bar represents the patient who was infected with CRAB before NSICU admission HAI. Molecular typing results revealed that all 5 strains results showed that CRAB isolated from the faucet aer- belonged to the same clone and this cloned strain caused ator and CRAB isolated from the clinical specimens had the outbreak, as shown in Fig. 4. the same cloned strain. Previous studies have discussed the role of faucet aerators as a reservoir for bacteria [22, Hand hygiene compliance 23]. Weber and Kappstein concluded that low-level con- The hand hygiene monitoring team conducted a hand tamination of potable water led to contamination of the hygiene compliance observation on December 26, 2018 faucet aerators with subsequent bacterial amplification in the NSICU. Compared with the other months in [24, 25]. But in Wang’s study, pathogens were thought to 2018, the hand hygiene compliance rate in December contaminate the faucet when it was used by the medical was at a lower level, which was lower than the annual staff, rather than contaminating the water supply system average of 74.15%, as shown in Fig. 5. [12]. It was difficult to determine whether the primary source of faucet contamination was municipal water, pipe- Discussion line, or the hands of the medical staff. In our study, based In the present study, environmental microbial sampling on the analysis of sampling results and hand hygiene results showed that potable water and the inner surface compliance results, we believed that contamination of the of the proximal end of the water outlet tested negative faucet aerators might have occoured from splashes origin- for CRAB, and only one isolate from the faucet aerator ating from handwasing by the HCWs, instead of low-level was found to be culture positive. The molecular typing contamination of potable water. It should be emphasized that because HCWs used the contaminated faucet to wash their hands, new cases of infection and colonization oc- curred on the 3rd and 4th day after the emergency re- sponse, with an interval of more than 48 h. Horcajada concluded that when a faucet is contaminated, contact precautions can fail, because HCWs wash their hands with contaminated water [26]. Successful control of the out- break by prohibiting the use of aerators also supported our hypothesis that a contaminated aerator played the role of a key environmental reservoir during the outbreak.. In our NSICU, traditional mechanical foot-operated fau- cets are used instead of electronic sensor faucets. The aer- ators of these faucets are made of several wire meshes to filter impurities in water and to prevent splashing. How- Fig. 3 Photograph of the faucet aerator. The faucet aerators are ever, these wires provide space for the propagation of made of several wire mesh to filter impurities in water and pathogenic microorganisms. Walker’sresearchshowed prevent splashing that the presence and type of aerator on the faucet was a Lv et al. Antimicrobial Resistance and Infection Control (2019) 8:205 Page 6 of 9 Table 1 Results of unadjusted conditional logistic regression modeling of the possible risk factors for CRAB acquisition by cases and controls in the neurosurgical intensive care unit (NSICU) Possible risk factor Case patients Control patients Univariate OR P (n =6) (N = 12) (95% CI) Blood transfusion or the use of blood products 2 (33.33%) 5 (41.67%) 0.70 (0.09–5.43) 1.000 Urinary catheterization 6 (100.00%) 12 (100.00%) …… Hemodialysis 0 (0.00%) 0 (0.00%) …… Venous catheterization 6 (100.00%) 6 (50.00%) … 0.054 Mechanical ventilation 5 (83.33%) 8 (66.67%) 2.50 (0.21–29.26) 0.615 Tracheotomy 5 (83.33%) 6 (50.00%) 5.00 (0.44–56.62) 0.316 Hypertension 5 (83.33%) 5 (41.67%) 7.00 (0.61–79.87) 0.152 Diabetes 0 (0.0%) 1 (8.33%) … 1.000 Chronic obstructive pulmonary disease 1 (16.67%) 0 (0.00%) … 0.333 Tumor 0 (0.00%) 0 (0.00%) …… Surgery 4 (66.67%) 4 (33.33%) 0.25 (0.03–2.00) 0.191 Medical group 3 (50.00%) 7 (58.33%) 0.71 (0.10–5.12) 0.738 NOTE. Data are no. (%) of objects. CI: confidence interval; OR: odds ratio ORs and 95% CIs for partial factors cannot be estimated, because the rate of these variables in the case or control was 0 or 100% Hypertensive patients were defined as those who had a systolic blood pressure ≥ 140 mmHg and/or diastolic blood pressure ≥ 90 mmHg [21] factor involved in water contamination [27]. In high-risk found only in the dining room, which was a busy room areas, Kappstein recommend either the removal of aera- with a greater amount of staff traffic than in other areas, tors or use of aerators without wire meshes that do not and the faucet was used frequently for hand washing. We collect sediments or lead to water stagnation, and regular believed that the faucet aerator was contaminated by cleaning of aerators [25]. In view of the use of the aerator splashes originating from handwashing by the HCWs,and it and the structure of the aerator, which might cause aggra- might have become an environmental reservoir of CRAB vated pollution, we believed that the management of fau- during the outbreak. Subsequently, during the hand wash- cet aerators in high-risk areas, such as the NSICU, should ing process, the CRAB-colonized faucet contaminated the be given greater attention. hands of the HCWs, which became the carrier of CRAB The aggregation of CRAB detection time in these and spread CRAB to the ICU inpatients. Patients in the NSICU patients was obvious, but the spatial distribution NSICU often have coma or confusion, and they need to of beds was more dispersed. The case-control study stay in bed for a long time. Compared with other ICU pa- showed that risk factors, such as medical group, invasive tients, there are more instances of tracheal opening and operation, and underlying diseases, were not the sus- assisted suction, and the risk of HAI is greater; even low- pected causes of the outbreak. The outbreak strain was level contamination can result in HAI [28, 29]. A. Fig. 4 Gel map by CHEF-Mapper PFGE analysis of 5 CRAB isolates from clinical and environmental samples. P2,P4,P10,P21: bed number of inpatients; FA: faucet aerator Lv et al. Antimicrobial Resistance and Infection Control (2019) 8:205 Page 7 of 9 Fig. 5 Hand hygiene compliance rate from January 2018 to January 2019 in NSICU. The hand hygiene compliance rate in December 2018 was at a low level throughout the year. Hand hygiene compliance monitoring happened to be done before the outbreak. baumannii was the main challenge in HAI prevention and This led to failure to understand the situation when the control in our NSICU. Its carbapenem-resistance rate NSICU was the most contaminated. In addition, we used reached 92.70%, and the isolation rate was 40.37% [30]. only pre-moistened cotton swabs for sampling, and we The bacterial reservoir (faucet aerator), the route of did not use sampling sponges, whose better capture abil- transmission (hands of the HCWs), and the suscep- ity had been confirmed in previous studies [35, 36]. tible population (NSICU inpatients) constitute the We did not sample the hands of the HCWs after they CRAB transmission chain in the outbreak. washed them under the contaminated faucet in the din- We used a set of emergency response procedures de- ing room, and we sampled only the hands of the medical veloped by our own hospital to discover and successfully staff that was undergoing medical treatment. Therefore, contain the outbreak in a timely manner. It was difficult in the chain hypothesis of CRAB transmission, we could to operate by simply using the “incidence above the pre- only infer from the results of hand hygiene compliance, vious level” mentioned in the guideline as a standard for and there was a lack of the most direct evidence. the emergency response [14], because occasionally it was We suggest that environmental sampling should be not easy to judge HAI cases, and doctors often needed carried out as much as possible before the implementa- to use the efficacy of antibiotics to assist in the judg- tion of emergency measures in future CRAB outbreak ment, but the timeliness of the emergency response investigations to obtain more abundant clues for patho- could not withstand such long delays. In addition, our gen transmission. previous research showed that positive detection of A. baumannii in patients has a distinct seasonal distribu- Conclusion tion [31], which has been discussed in many previous This study highlights the importance of faucet aerators. studies [32–34]. The incidence of HAIs caused by A. In high-risk areas, we recommend that faucet aerators baumannii differs with seasonal changes, and therefore, should not be used during an outbreak or they should it is not appropriate to judge whether HAI outbreaks be disassembled and cleaned. may occur according to the morbidity level. We believe that a sensitive emergency response initiation standard is the key to controlling HAI outbreaks. This standard Supplementary information may only be suitable for use in our own ICU, as it is Supplementary information accompanies this paper at https://doi.org/10. based on our long-term experience in dealing with HAI 1186/s13756-019-0635-y. outbreaks in our ICU (Additional file 1), which has its own unique architectural layout, bed layout, and infec- Additional file 1. Background epidemiology of the NSICU and recent HAI outbreaks tion control features. Although the suitability of this standard may be limited, our approach can provide other hospitals with a new way of strategizing to control HAI outbreaks. Abbreviations CHINET: China Antimicrobial Surveillance Network; CRAB: Carbapenem- Study limitations resistant Acinetobacter baumannii; GCS: Glasgow Coma Scale; HAI: Healthcare-associated infection; HCWs: Healthcare workers; Because the intensive infection control measures were NHSN: National Healthcare Safety Network; NSICU: Neurosurgical intensive carried out before environmental microbial sampling, care unit; PFGE: Pulsed-Field Gel Electrophoresis; RIT: Repeat Infection only one positive environmental specimen was detected. Timeframe; WHO: World Health Organization Lv et al. Antimicrobial Resistance and Infection Control (2019) 8:205 Page 8 of 9 Acknowledgements 9. Knoester M, De Boer MGJ, Maarleveld JJ, et al. An integrated approach We are grateful to Fupin Hu (Huashan Hospital Fudan University) for helping to control a prolonged outbreak of multidrug-resistant Pseudomonas us complete the molecular typing work. We thank LetPub (www.letpub.com) aeruginosa in an intensive care unit. 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Antimicrobial Resistance & Infection Control – Springer Journals
Published: Dec 30, 2019