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Identification and Infection Control of Carbapenem-Resistant Enterobacterales in Intensive Care Units

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Identification and Infection Control of Carbapenem-Resistant Enterobacterales in Intensive Care Units Acute and Critical Care 2021 August 36(3):175-184 Acute and Critical Care https://doi.org/10.4266/acc.2021.00409 | pISSN 2586-6052 | eISSN 2586-6060 Identification and infection control of carbapenem- resistant Enterobacterales in intensive care units Jongyoun Yi1,2, Kye-Hyung Kim2,3 1Department of Laboratory Medicine, Pusan National University School of Medicine, Busan; 2Medical Research Institute, Pusan National University Hospital, Busan; 3Department of Internal Medicine, Pusan National University School of Medicine, Busan, Korea Infections with multidrug-resistant organisms among patients in intensive care units (ICUs) are associated with high mortality. Among multidrug-resistant organisms, carbapenem-resis- Review Article tant Enterobacterales (CRE) harbor important pathogens for healthcare-associated infections, including pneumonia, bacteremia, and urinary tract infections. Risk factors for CRE coloniza- Received: April 5, 2021 Revised: June 10, 2021 tion include underlying comorbid conditions, prior antibiotics exposure, prior use of health- Accepted: June 14, 2021 care facilities, device use, and longer ICU stay. The mortality rate due to invasive CRE infec- tion is 22%–49%, and CRE colonization is associated with an approximately 10-fold increased Corresponding author risk of CRE infection. Infection control measures include hand hygiene, contact precautions, Kye-Hyung Kim minimizing the use of devices, and environmental control. Additionally, implementing active Department of Internal Medicine, Pusan National University School of surveillance of CRE carriage should be considered in ICU settings. Medicine, 179 Gudeok-ro, Seo-gu, Busan 49241, Korea Key Words: carbapenem; carbapenem-resistant enterobacteriaceae; drug resistance; infec- Tel: +82-51-240-7735 tion control; intensive care units Fax: +82-51-254-3127 E-mail: [email protected] INTRODUCTION Patients in intensive care units (ICUs) are susceptible to nosocomial infections due to under- lying diseases, device use, and prior antibiotics use. Nosocomial infections are associated with morbidity, mortality, and increased costs [1,2]. An international study conducted in 1,265 ICUs from 75 countries showed that 51% (7,087/13,796) of patients were considered having infection according to the definitions of the International Sepsis Forum, and 71% were receiving antibiotics. Additionally, the infection rate of ICU patients was related to disease se- verity, and infection was independently associated with a greater risk of hospital mortality (adjusted odds ratio, 1.51; 95% confidence interval, 1.36–1.68; P<0.001) [2]. ICU patients are at a high risk of colonization and infection caused by multidrug-resistant organisms (MDROs). Patients with extended ICU stays have higher rates of infection by resis- tant organisms [2]. MDROs, including methicillin-resistant Staphylococcus aureus, vancomy- Copyright © 2021 The Korean Society cin-resistant enterococci (VRE), multi-drug resistant Acinetobacter baumannii (MRAB), and of Critical Care Medicine This is an Open Access article distributed Enterobacterales that produce extended-spectrum β-lactamases (ESBL), are associated with under the terms of Creative Attributions ICU-related nosocomial infections [3]. Of these MDROs, Enterobacterales, an order of Gram- Non-Commercial License (https:// creativecommons.org/li-censes/by-nc/4.0/) negative bacteria, harbor common pathogens for healthcare-associated infections, including which permits unrestricted noncommercial use, distribution, and reproduction in any pneumonia, bacteremia, and urinary tract infections. Recently, among MDROs, carbapen- medium, provided the original work is properly cited. em-resistant Enterobacterales (CRE) have emerged as a threat for ICU patients [4] because of https://www.accjournal.org 175 Yi J, et al. CRE infection in ICUs limited treatment options and high mortality rates [5]; there- KEY MESSAGES fore, CRE outbreaks, especially in the ICU, have become a crit- ical issue. Several agents including ceftazidime-avibactam, ■ Due to limited treatment options, invasive carbapenem- resistant Enterobacterales (CRE) colonization and in- ceftolozane-tazobactam, meropenem-vaborbactam, and imi- fection in critically ill patients are associated with high penem-cilastatin-relebactam have been approved for clinical mortality. use [5], but these agents are not available in Korea. This study ■ The prevalence of CRE and carbapenemase-producing presents a review of the epidemiology, risk factors, clinical CRE continues to increase. outcomes, and infection control of CRE in the ICU setting. ■ Infection control measures, including hand hygiene, con- tact precaution, environmental control, and active sur- DEFINITION OF CRE veillance should be implemented to reduce mortality due to CRE infection. The Centers for Disease Control and Prevention (CDC) de- fines CRE as: (1) Enterobacterales that test resistant to at least one of the carbapenem antibiotics (i.e., minimum inhibitory can be found in various Enterobacterales, including Escherich- concentrations of ≥4 µg/mL for doripenem, meropenem, and ia coli, Citrobacter spp., Serratia marcescens, and Enterobacter imipenem, and ≥2 µg/mL for ertapenem) or (2) Enterobacte- spp. [12,14-17]. Clinically significant Class B carbapenemases rales that produce a carbapenemase [6]. For Enterobacterales are IMP (active on imipenem), Verona integron-encoded me- (Proteus species, Morganella spp., Providencia spp.) that may tallo-β-lactamase, and New Delhi metallo-β-lactamase (NDM) have intrinsic reduced susceptibilities to imipenem other car- [10,12]. Class D carbapenemases are referred to as OXA car- bapenem antibiotics should be used to test carbapenem re- bapenemases due to their ability to hydrolyze oxacillin; OXA sistance [6]. stands for oxacillinase [18]. There are many different variants The “E” in CRE used to stand for the family Enterobacteria- or subtypes of carbapenemases, from KPC-1 to KPC-67, ac- ceae but has been recently altered to the order Enterobactera- cording to the order reported and amino acid substitutions les due to taxonomic changes [7]. If the older usage (Entero- [19-21]. bacteriaceae) is to be persistently held, important genera like Proteus, Serratia, and Pantoea, despite their infrequent resis- EPIDEMIOLOGY OF CRE tance to carbapenems, will be omitted from CRE. The prevalence of CRE infection continues to increase global- CARBAPENEMASES ly [8]. In the United States, an active surveillance study showed that the overall annual incidence of CRE infection was 2.93 One mechanism of resistance to carbapenem antibiotics in cases per 100,000 persons in seven U.S. metropolitan commu- Enterobacterales is the production of carbapenemases, the nities, and site-specific incidence rates ranged from 0.35 to enzymes that hydrolyze carbapenem antibiotics and are en- 4.58 per 100,000 persons [22]. In a 2019 report, 13,100 cases of coded by mobile genetic elements [8]. Approximately 30% of CRE infection were reported in the U.S., with 1,100 hospital- CRE are carbapenemase-producing CRE (CPE) that harbor ized patients deaths [23]. The first CPE reported was KPC-pro- the carbapenemases [9], which rapidly spread resistance [8]. ducing K. pneumoniae from North Carolina in 1996 [24], and The Ambler classification system, which is based on amino by 2001, many reports of CPE from the northeastern U.S. had acid homology, shows four major classes of β-lactamases, viz., been published [25]. KPC-producing K. pneumoniae is mostly classes A, B, C, and D [10,11]. Classes A, C, and D β-lactamases found in North America, Israel, Latin America, Italy, and Greece share a serine residue in their active site (serine β-lactamases), (Table 1) [8,25]. A CRE network study conducted in China in while class B β-lactamases require zinc for their action (metal- 2015 reported that the overall incidence of CRE infection was lo-beta-lactamases, MBLs) [12,13]. Classes A, B, and D confer 4.05 per 100,000 patient-days (from 0.32 in Qinghai to 14.38 in carbapenem resistance in Enterobacterales and have clinical Jiangsu), and 20.8% of CRE-infected patients were admitted to importance for their role as healthcare-associated pathogens the ICU [26]. A study comprising active screening of CRE in- [5,12]. Clinically, the most significant class A carbapenemase fections in hematology units in China reported that the CRE is the Klebsiella pneumoniae carbapenemase (KPC) group [8]. colonization rate in patients was 16.46% [27]. In a prospective Owing to the transmission from Klebsiella to other genera, KPC cohort study of inpatients from the ICU and hematopoietic 176 https://www.accjournal.org Acute and Critical Care 2021 August 36(3):175-184 Yi J, et al. CRE infection in ICUs Table 1. Clinically important carbapenemases in healthcare-associated pathogens and their classification, species distributions, and epide- miology [8,12] Carbapenemases class Major Characteristic Major endemic areas or areas with regional spread (Ambler classification) carbapenemase A Serine beta-lactamases KPC North America, Latin America, Israel, Italy, Greece, China, Korea B Metallo-beta-lactamases NDM India, Pakistan, Bangladesh, China IMP India, Japan, Taiwan, Greece VIM India, Greece, Italy D Serine beta-lactamases OXA France, Netherlands, Germany, Spain, Malta, Middle East, Morocco KPC: Klebsiella pneumoniae carbapenemase; NDM: New Delhi metallo-β-lactamase; IMP: active on imipenem; VIM: Verona integron-encoded metallo- β-lactamase; OXA: oxacillinase. Table 2. Risk factors for colonization of CRE
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