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      Increase in Hospital-Acquired Carbapenem-Resistant Acinetobacter baumannii Infection and Colonization in an Acute Care Hospital During a Surge in COVID-19 Admissions — New Jersey, February–July 2020

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          Abstract

          On December 1, 2020, this report was posted online as an MMWR Early Release. Carbapenem-resistant Acinetobacter baumannii (CRAB), an opportunistic pathogen primarily associated with hospital-acquired infections, is an urgent public health threat ( 1 ). In health care facilities, CRAB readily contaminates the patient care environment and health care providers’ hands, survives for extended periods on dry surfaces, and can be spread by asymptomatically colonized persons; these factors make CRAB outbreaks in acute care hospitals difficult to control ( 2 , 3 ). On May 28, 2020, a New Jersey hospital (hospital A) reported a cluster of CRAB infections during a surge in patients hospitalized with coronavirus disease 2019 (COVID-19). Hospital A and the New Jersey Department of Health (NJDOH) conducted an investigation, and identified 34 patients with hospital-acquired multidrug-resistant CRAB infection or colonization during February–July 2020, including 21 (62%) who were admitted to two intensive care units (ICUs) dedicated to caring for COVID-19 patients. In late March, increasing COVID-19–related hospitalizations led to shortages in personnel, personal protective equipment (PPE), and medical equipment, resulting in changes to conventional infection prevention and control (IPC) practices. In late May, hospital A resumed normal operations, including standard IPC measures, as COVID-19 hospitalizations decreased, lessening the impact of personnel and supply chain shortages on hospital functions. CRAB cases subsequently returned to a pre–COVID-19 baseline of none to two cases monthly. The occurrence of this cluster underscores the potential for multidrug-resistant organisms (MDROs) to spread during events when standard hospital practices might be disrupted; conventional IPC strategies should be reinstated as soon as capacity and resources allow. Hospital A is an urban, acute-care hospital in New Jersey with approximately 500 beds. In May 2020, hospital A notified NJDOH of an increase in CRAB (A. baumannii with meropenem minimum inhibitory concentration testing of ≥8 μg/mL) isolates from weekly ICU point prevalence surveys (colonization screening) and from clinical infections. Hospital A retrospectively reviewed microbiology records for CRAB isolated from inpatient specimens since November 2019 and instituted prospective surveillance of laboratory results to identify all CRAB isolates. Inpatients with hospital-acquired CRAB infection were defined as those for whom CRAB was isolated from clinical or colonization screening specimens collected on or after hospital day 3 and who had no earlier CRAB isolated from specimens during the same hospitalization; incident CRAB was a patient‘s first CRAB infection or colonization. Patients’ demographic characteristics, diagnoses, treatments, disposition, and COVID-19 status were collected from medical records. Diagnoses of CRAB infection or colonization were determined by infectious disease specialists. NJDOH began an investigation to assess IPC practices at hospital A and gather additional data. This activity was reviewed by CDC and was conducted consistent with applicable federal law and CDC policy.* During February–July 2020, 34 patients with hospital-acquired CRAB infection or colonization were identified, including 28 (82%) whose incident CRAB infection or colonization occurred during the facility’s surge in COVID-19 cases (March–June 2020) (Figure), and 17 (50%) who had confirmed infection with SARS-CoV-2, the virus that causes COVID-19 (Table). Twenty (59%) incident cases were identified from clinical specimens and 14 (41%) through colonization screening. Median age of patients with CRAB infection was 55 years (interquartile range [IQR] = 48–64 years), and 28 patients (82%) were admitted from home. No patients had prior documented CRAB infection or colonization. The median interval from admission to incident CRAB infection was 19 days (IQR = 11–28 days). Twenty-five (74%) patients were intubated and mechanically ventilated at the time of specimen collection; those with COVID-19 were placed in a prone position. CRAB infection was diagnosed in 20 (59%) of the 34 patients, including 14 (41%) with clinically diagnosed CRAB ventilator-associated pneumonia, four of whom had bacteremia. At the time of this report, 23 (68%) patients with CRAB infection had been discharged, 10 (29%) had died, and one remained hospitalized. FIGURE Number of admitted patients with COVID-19 (N = 846) and hospital-acquired carbapenem-resistant Acinetobacter baumannii (CRAB)* (N = 34), by month — hospital A, New Jersey, February–July 2020 Abbreviation: COVID-19 = coronavirus disease 2019. * CRAB infection or colonization. The figure is a combination bar and line graph showing the number of admitted patients with COVID-19 (N = 846)and hospital-acquired carbapenem-resistant Acinetobacter baumannii (N = 34)at hospital A in New Jersey during February–July 2020, by month. TABLE Demographic and clinical characteristics of patients with carbapenem-resistant Acinetobacter baumannii (CRAB) (N = 34) — hospital A, New Jersey, February–July 2020 Characteristics of patients with CRAB No. (%) of patients Age, median (IQR), yrs 55 (48–64) Sex Male 24 (71) Female 10 (29) Location before admission Home 28 (82) Skilled nursing facility 5 (15) Long-term acute care hospital 1 (3) Collection location of incident CRAB Intensive care unit 25 (73) Medical-surgical unit 5 (15) Progressive care or step-down unit 4 (12) Specimen source of incident CRAB Respiratory (sputum, tracheal aspirate, or bronchial) 17 (50) Axilla, groin, or rectal 6 (18) Blood 5 (15) Wound, bone, or other tissue 4 (12) Urine 2 (5) SARS-CoV-2 status Positive 17 (50) Negative 17 (50) CRAB infection/colonization Ventilator-associated pneumonia 10 (29) Ventilator-associated pneumonia with bacteremia 4 (12) Bacteremia 3 (9) Bone or soft tissue infection 3 (9) Colonization 14 (41) Intubation/Mechanical ventilation at time of incident CRAB Yes 25 (74) No 7 (21) Tracheostomy Yes 8 (24) No 26 (76) Received respiratory therapy services Yes 28 (82) No 6 (18) Disposition Discharged/Transferred 23 (68) Deceased 10 (29) Remains hospitalized 1 (3) Abbreviation: IQR = interquartile range The multidrug-resistant CRAB definition (A. baumannii with documented resistance to three or more classes of antibiotics) was applied to hospital clinical laboratory antimicrobial susceptibility data for incident cases ( 4 ); all 34 met multidrug-resistant CRAB criteria. Thirty isolates were further evaluated for carbapenemase genes through real-time polymerase chain reaction testing. † Twenty-six isolates harbored the gene encoding the OXA-23 carbapenemase. Among these isolates, two from specimens collected in February and March harbored an additional carbapenemase gene, encoding New Delhi metallo-β-lactamase (a gene rarely present in CRAB isolates from patients in the United States), indicating that at least one CRAB introduction occurred before the surge of COVID-19 cases ( 5 ). Four specimens were nonviable or did not yield CRAB growth. During March–August 2020, hospital A admitted approximately 850 patients with COVID-19. The number of cases peaked on April 9, with 36 new hospitalizations and 61% of the inpatient census having a diagnosis of confirmed or suspected COVID-19. Pandemic-related resource challenges necessitated intentional changes to IPC measures. Before the pandemic, ventilator circuits and suctioning catheters were changed at specified intervals of every 14 days and every 3 days, respectively, unless malfunctioning or visibly soiled. To conserve equipment during the surge, the hospital’s respiratory therapy unit instituted a policy to extend the use of ventilator circuits and suctioning catheters for individual patients, replacing them only if they were visibly soiled or malfunctioning. To conserve PPE, gown use as part of Contact Precautions§ was suspended for care of patients with the endemic MDROs vancomycin-resistant Enterococcus spp. and methicillin-resistant Staphylococcus aureus ¶ but was maintained for nonendemic MDROs such as CRAB. Gowns and gloves continued to be used for all patients when indicated for Standard Precautions, including wearing a gown when skin or clothing was likely to be exposed to blood or body fluids.** Anticipating shortages, hospital A also adopted an extended-use PPE protocol for N95 respirators and face shields. To prioritize personnel resources, activities of the MDRO workgroup, a multidisciplinary team responsible for guiding IPC policy around MDRO prevention efforts at hospital A, were suspended, along with biweekly bedside central venous catheter and indwelling urinary catheter maintenance rounds. Routine audits of appropriate PPE use, hand hygiene compliance, and environmental cleaning were also temporarily discontinued. Responding to COVID-19–related care needs also resulted in other unintentional changes in standard practices for preventing the spread of MDROs and device-associated infections. IPC leadership noted less frequent patient bathing with chlorhexidine gluconate and a 43% reduction in ICU CRAB screening tests. These changes resulted from competing clinical priorities, challenges in personnel availability, and an effort to minimize staff members’ interaction time with patients. The facility experienced critical shortages in personnel for nursing and environmental services, resulting from staff members’ illness, quarantine, and a surge in the number of patients with COVID-19. Nursing resources were supplemented through agency and government entities; however, increased patient-to-staff member ratios and the need to minimize patient contact might have led to unidentified IPC breaches. In early May, hospital A’s IPC leadership advised physicians, unit managers, and environmental services of the CRAB cluster. Environmental services cleaned common areas and high-touch surfaces of ICUs with bleach. Proper hand hygiene and PPE use were reinforced through unit-based education, and compliance audits were restarted by mid-May. At the end of May, environmental services terminally cleaned and disinfected the COVID-19 dedicated ICUs and associated portable medical and respiratory equipment. IPC personnel and unit leadership reinforced CRAB surveillance culture protocol adherence. Public Health Response In collaboration with hospital A, NJDOH investigated the cluster, including review of laboratory data, patient information, IPC policies, and audit tools. NJDOH provided technical guidance on IPC interventions and advised returning to normal operations as soon as capacity allowed. IPC processes and interventions developed in collaboration with NJDOH (adapted from CDC guidelines †† ) during a previous CRAB outbreak at hospital A helped establish metrics for baseline incident case counts and adherence to IPC-related measures. In June, NJDOH used New Jersey’s public health notification system §§ to alert public health officials, health care providers, and infection preventionists to the possible resurgence of MDROs in health care facilities facing COVID-19–related resource limitations. In June 2020, hospital A reported fewer incident hospital-associated CRAB cases, coinciding with a sharp decrease in COVID-19 hospitalizations (Figure). This trend continued through July. In August, no incident hospital-associated CRAB cases were reported, signaling a return to baseline numbers for the facility. Discussion The impact of the COVID-19 pandemic on the spread of antibiotic resistance in health care settings has not been fully described. In response to a rapid increase in SARS-CoV-2 infections, many health care facilities adopted mitigation strategies to contend with physical space limitations, constrained availability of personnel, shortages in PPE, and a large number of critically ill patients. Recent single-facility reports from the United States and Europe have described increased acquisition of MDROs among patients hospitalized with COVID-19 ( 6 – 8 ). Hospital A experienced a large multidrug-resistant CRAB outbreak, primarily involving ICU patients, which extended across multiple units during a surge in COVID-19 cases. Outbreaks of CRAB have been well documented in acute care hospitals, particularly among critically ill patients, and are often driven by factors that include breaches in infection control and persistent environmental contamination ( 3 , 9 ). Containing these outbreaks often requires multiple, targeted interventions, including increased surveillance, IPC audits, and environmental cleaning ( 10 ). During COVID-19 preparations and the ensuing surge in cases, decreased vigilance for control of CRAB transmissions, including suspension of the MDRO workgroup, reduced surveillance cultures, reduced personnel numbers (which decreased capacity for overall auditing practices), and both intentional and unintentional changes in IPC practice likely contributed to this CRAB cluster. The lack of audits made identifying and correcting real-time IPC compliance issues difficult. Diminished colonization screening might have resulted in a higher threshold for recognizing increasing incident hospital-acquired CRAB cases. Reinstatement of conventional IPC strategies in ICUs, paired with enhanced cleaning procedures and hand hygiene reeducation, likely contributed to the rapid decline in cases. The findings in this report are subject to at least three limitations. First, CRAB can colonize persons for long periods, possibly leading to misclassification of some cases present at admission as hospital-acquired cases; decreased ICU surveillance testing might have contributed to this misclassification. Second, objective assessment of hand hygiene, PPE use, and environmental cleaning during the surge in COVID-19 cases is difficult without routine audit data. Finally, whole genome sequencing to determine the relatedness of isolates was not performed. Carbapenem resistance mechanism testing indicated at least two introductions of CRAB, including one preceding the surge. Whether OXA-23 CRAB spread into distinct patient populations (i.e., patients with and without COVID-19) or these were different introductions remains unclear. The COVID-19 pandemic has required hospitals to take unprecedented measures to maintain continuity of patient care and protect health care personnel from infection. This outbreak highlights that MDROs can spread rapidly in hospitals experiencing surges in COVID-19 cases and cause serious infections in this setting. To reduce spread of MDROs and the risk of infection for patients, hospitals should remain vigilant to prevent and detect clusters of unusual infections and respond promptly when they are detected. Facilities should prioritize continuity of core IPC practices (e.g., training for and auditing of hand hygiene, PPE use, and environmental cleaning) to the greatest extent possible during surges in hospitalizations and make every effort to return to normal operating procedures as soon as capacity allows. Summary What is already known about this topic? Carbapenem-resistant Acinetobacter baumannii (CRAB) causes health care–associated infections that are challenging to contain and often linked to infection prevention and control (IPC) breaches. What is added by this report? A New Jersey hospital reported a cluster of 34 CRAB cases that peaked during a surge in COVID-19 hospitalizations. Strategies to preserve continuity of care led to deviations in IPC practices; CRAB cases decreased when normal operations resumed. What are the implications for public health practice? Hospitals managing surges of patients with COVID-19 might be vulnerable to outbreaks of multidrug-resistant organism (MDRO) infections. Maintaining IPC best practices (e.g., MDRO surveillance and hand hygiene and environmental cleaning audits) to the extent possible could mitigate spread.

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          Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance.

          Many different definitions for multidrug-resistant (MDR), extensively drug-resistant (XDR) and pandrug-resistant (PDR) bacteria are being used in the medical literature to characterize the different patterns of resistance found in healthcare-associated, antimicrobial-resistant bacteria. A group of international experts came together through a joint initiative by the European Centre for Disease Prevention and Control (ECDC) and the Centers for Disease Control and Prevention (CDC), to create a standardized international terminology with which to describe acquired resistance profiles in Staphylococcus aureus, Enterococcus spp., Enterobacteriaceae (other than Salmonella and Shigella), Pseudomonas aeruginosa and Acinetobacter spp., all bacteria often responsible for healthcare-associated infections and prone to multidrug resistance. Epidemiologically significant antimicrobial categories were constructed for each bacterium. Lists of antimicrobial categories proposed for antimicrobial susceptibility testing were created using documents and breakpoints from the Clinical Laboratory Standards Institute (CLSI), the European Committee on Antimicrobial Susceptibility Testing (EUCAST) and the United States Food and Drug Administration (FDA). MDR was defined as acquired non-susceptibility to at least one agent in three or more antimicrobial categories, XDR was defined as non-susceptibility to at least one agent in all but two or fewer antimicrobial categories (i.e. bacterial isolates remain susceptible to only one or two categories) and PDR was defined as non-susceptibility to all agents in all antimicrobial categories. To ensure correct application of these definitions, bacterial isolates should be tested against all or nearly all of the antimicrobial agents within the antimicrobial categories and selective reporting and suppression of results should be avoided. © 2011 European Society of Clinical Microbiology and Infectious Diseases. No claim to original US government works.
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            Antimicrobial Stewardship Program, COVID-19, and Infection Control: Spread of Carbapenem-Resistant Klebsiella Pneumoniae Colonization in ICU COVID-19 Patients. What Did Not Work?

            The Italian burden of disease associated with infections due to antibiotic-resistant bacteria has been very high, largely attributed to Carbapenem-Resistant Klebsiella pneumoniae (CR-Kp). The implementation of infection control measures and antimicrobial stewardship programs (ASP) has been shown to reduce healthcare-related infections caused by multidrug resistance (MDR) germs. Since 2016, in our teaching hospital of Terni, an ASP has been implemented in an intensive care unit (ICU) setting, with the “daily-ICU round strategy” and particular attention to infection control measures. We performed active surveillance for search patients colonized by Carbapenem-Resistant Enterobacteriaceae (CRE). In March 2020, coronavirus disease 2019 (COVID-19) arrived and the same ICU was reserved only for COVID-19 patients. In our retrospective observational study, we analyzed the bimonthly incidence of CRE colonization patients and the incidence of CRE acquisition in our ICU during the period of January 2019 to June 2020. In consideration of the great attention and training of all staff on infection control measures in the COVID-19 era, we would have expected a clear reduction in CRE acquisition, but this did not happen. In fact, the incidence of CRE acquisition went from 6.7% in 2019 to 50% in March–April 2020. We noted that 67% of patients that had been changed in posture with prone position were colonized by CRE, while only 37% of patients that had not been changed in posture were colonized by CRE. In our opinion, the high intensity of care, the prone position requiring 4–5 healthcare workers (HCWs), equipped with personal protective equipment (PPE) in a high risk area, with extended and prolonged contact with the patient, and the presence of 32 new HCWs from other departments and without work experience in the ICU setting, contributed to the spread of CR-Kp in our ICU, determining an increase in CRE acquisition colonization.
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              Control of Carbapenem-resistant Enterobacteriaceae, Acinetobacter baumannii , and Pseudomonas aeruginosa in Healthcare Facilities: A Systematic Review and Reanalysis of Quasi-experimental Studies

              Abstract Carbapenem-resistant Enterobacteriaceae (CRE), Acinetobacter baumannii (CRAB), and Pseudomonas aeruginosa (CRPsA) are a serious cause of healthcare-associated infections, although the evidence for their control remains uncertain. We conducted a systematic review and reanalysis to assess infection prevention and control (IPC) interventions on CRE-CRAB-CRPsA in inpatient healthcare facilities to inform World Health Organization guidelines. Six major databases and conference abstracts were searched. Before-and-after studies were reanalyzed as interrupted time series if possible. Effective practice and organization of care (EPOC) quality criteria were used. Seventy-six studies were identified, of which 17 (22%) were EPOC-compatible and interrupted time series analyses, assessing CRE (n = 11; 65%), CRAB (n = 5; 29%) and CRPsA (n = 3; 18%). IPC measures were often implemented using a multimodal approach (CRE: 10/11; CRAB: 4/5; CRPsA: 3/3). Among all CRE-CRAB-CRPsA EPOC studies, the most frequent intervention components included contact precautions (90%), active surveillance cultures (80%), monitoring, audit and feedback of measures (80%), patient isolation or cohorting (70%), hand hygiene (50%), and environmental cleaning (40%); nearly all studies with these interventions reported a significant reduction in slope and/or level. The quality of EPOC studies was very low to low.
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                Author and article information

                Journal
                MMWR Morb Mortal Wkly Rep
                MMWR Morb Mortal Wkly Rep
                WR
                Morbidity and Mortality Weekly Report
                Centers for Disease Control and Prevention
                0149-2195
                1545-861X
                04 December 2020
                04 December 2020
                : 69
                : 48
                : 1827-1831
                Affiliations
                Epidemic Intelligence Service, CDC; Communicable Disease Service, New Jersey Department of Health; Division of Healthcare Quality Promotion, National Center for Emerging and Zoonotic Infectious Diseases, CDC; New Jersey Medical School, Rutgers University, Newark, New Jersey.
                Author notes
                Corresponding author: Stephen Perez, okm9@ 123456cdc.gov .
                Article
                mm6948e1
                10.15585/mmwr.mm6948e1
                7714028
                33270611
                3e11e378-90c7-45e3-a2f2-f51eebccb1b0

                All material in the MMWR Series is in the public domain and may be used and reprinted without permission; citation as to source, however, is appreciated.

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