key: cord-1005815-iof4s4zv
authors: Eckardt, Paula; Canavan, Kelsi; Guran, Rachel; George, Elizabeth; Miller, Nancimae; Avendano, Dianeysis H.; Kim, Myeongji; Himed, Khaled; Ramirez, Karen Heidi Gonzalez
title: Containment of a Carbapenem-resistant Acinetobacter baumanniii complex outbreak in a COVID-19 intensive care unit
date: 2022-02-26
journal: Am J Infect Control
DOI: 10.1016/j.ajic.2022.02.022
sha: 2fbe8f0f5b94cbf3a504c396260f8143d007fb2b
doc_id: 1005815
cord_uid: iof4s4zv

BACKGROUND: A Carbapenem-resistant Acinetobacter baumannii outbreak in the COVID intensive care unit of a community hospital was contained using multidrug resistant organism guidelines. The purpose of this study is to report on an outbreak investigation and containment strategy that was used, and to discuss prevention strategy. METHODS: A multidisciplinary approach contained the spread of infection. Strategies implemented included consultation with experts, screening, and reversal of personal protective equipment conservation. Ensuring infection control best practices are maintained remain important efforts to reduce the spread of MDROs. RESULTS: Five patients with CRAB were identified from routine clinical cultures within one week and one patient was identified from active surveillance cultures. DISCUSSION: PPE conservation, patient care strategies to prevent healthcare personnel exposure, and patient surge staffing protocols may have increased the likelihood of MDRO transmission. Environmental and behavioral infection control regulations with effective administrative guidance, active surveillance cultures, and antibiotic stewardship are critical to prevent future outbreaks. CONCLUSION: After outbreak containment strategies were implemented, no additional patients were identified with CRAB. Conventional infection prevention and control strategies were re-instituted. A multidisciplinary approach with continued focus on hand hygiene, environmental cleaning, and correct use of personal protective equipment needs to be put in place to successfully contain and prevent the spread of the serious public health threat of carbapenem resistant infections.

outbreak, containment, COVID, MDRO, Acinetobacter baumanni, antimicrobial resistance, infection prevention, PPE

The COVID-19 pandemic brought many challenges with regard to standard infection prevention practices and the proliferation of multi-drug resistant organisms (MDROs) (Polly et al., 2021; Rangel et al., 2021) . Several outbreaks of MDROs within COVID units have been described in the literature (Perez et al., 2020) . During the first few months of the pandemic, PPE availability worldwide was limited and the infection prevention practices were adjusted in order to maintain the access to PPE necessary for patient care. As a results of the acute need for PPE in healthcare and in the general population, the markets were depleted of the products necessary to protect healthcare workers from COVID-19 and other potential infectious diseases ( Acinetobacter baumannii is a gram-negative, strictly aerobic, non-fastidious, nonfermenting, catalase-positive, oxidase-negative opportunistic pathogen that is a challenging nosocomial pathogen that is an emerging public health threat (Balkhair et (CDC, 2019a). The threat level was escalated to "urgent" from "serious" in 2019 because of the emergence of its remarkable ability to upregulate or acquire foreign resistance determinants and the lack of current treatment options (CDC, 2019b). In 2017, 8,500 infections, 700 deaths, and 281 million dollars of healthcare costs were attributed to CRAB (CDC, 2019a). Along with antibiotic resistance, ability of A. baumannii to survive for prolonged periods in a hospital environment further potentiates nosocomial spread particularly in ICUs and long-term care facilities (Peleg & Hooper, 2010; Peleg et al., 2008) . The spread of infection can also be facilitated by health care personnel who are at increased risk of becoming contaminated with CRAB (Morgan et al., 2010) . The majority of patients who develop nosocomial CRAB infection have been exposed to a healthcare facility and have an indwelling device (Bulens et al., 2018) . In this study, we report a detailed investigation of a CRAB outbreak in the COVID intensive care unit (ICU) of a community hospital. We will discuss successful containment strategies that were utilized during the outbreak and will also discuss strategies to prevent future outbreaks.

The community hospital is a 176-bed acute care facility with an 18 bed ICU compromised of all private rooms with a centralized nursing station, medication room, and nutrition room. CRAB had not been previously identified in this ICU in the two years leading up to the outbreak and it has not been identified since the containment strategies were implemented (Table 2) . During the pandemic, the ICU was being used for critical care level COVID positive patients. Identification of an index patient with Carbapenem resistant A. baumanii in the COVID ICU in November 2020 prompted an outbreak investigation and mounted an immediate containment response. Upon identification of further patients, the outbreak management was expanded.

The response began with immediate closure to new admissions or transfers as well as cohorting of all exposed patients in the unit. Entry points were restricted in the ICU and staff entry was limited including consulting physicians utilizing telehealth. Positive CRAB patients were placed on a designated wing with dedicated nursing and respiratory staff. All patients that had been transferred out of the COVID ICU were maintained on contact transmission based precautions. The remaining patients in the ICU were considered potentially exposed and were moved to clean rooms but remained in the ICU until active surveillance cultures (ASC) resulted.

CRAB patients were placed on a new, expanded enhanced contact and respiratory transmission based precautions which included isolation gowns, gloves, and universal masks and eye protection. Gown conservation strategies that had been implemented due to anticipated PPE shortages caused by COVID-19 were immediately reversed. This change now required isolation gowns and gloves to be discarded after each patient encounter according to pre-pandemic conventional infection prevention and control practices.

Following the identification of multiple patients with CRAB in the ICU, containment began with planning point prevalence screenings using active surveillance cultures (ASC) on the remaining patients in the unit. Upon conducting a literature review it was determined that the best body site for screening for A. baumanii had not been well documented (Tacconelli et al., 2014) . After consulting with the hospital microbiology department, the infection prevention team determined that the best immediate action was to collect throat swabs from all patients within the COVID ICU. Since the initial positive clinical culture had been a sputum culture from a ventilated patient in the COVID ICU ward, it was thought that shared respiratory therapists within the ward may have been the source of transmission. Non-invasive groin and axilla screening had been described in the literature and was additionally performed after consultation with the local and state Department of Health and Centers for Disease Control and Prevention experts in order to identify additional potential cases (Buser et al., 2017) . While the most conclusive site of A. baumannii active surveillance screening has not been determined due to the low yield of single site collections, our study used the two different sites of both axilla and groin to assess for potential colonization (Buser et al., 2017; Nutman et al., 2020) . Two sites were agreed upon by the multidisciplinary team due to pandemic surge constraints in the laboratory.

Screening for new cases through ASC were performed on all patients in the unit as well as two additional hospital units that had received patient transfers before the COVID ICU was closed. Nurses were given specific instructions when collecting swab cultures, requiring 5 passes of the swab in each body location moving from axillae to groin. The initial point prevalence testing (PP#1) was multifaceted; initially throat swabs were collected on all patients in the COVID ICU as well as two patients that had been moved to the COVID telemetry ward (n=19).

One colonized patient was identified in the COVID-ICU. The following day, after consultation with the state, additional swabs of the axilla and groin were collected on the patients within the COVID ICU as well as non-COVID ICU (n=28) that shared respiratory, nursing and intensivist staff. A second point prevalence survey (PP#2) was conducted two weeks later with sputum cultures collected on all ventilated patients within both the COVID ICU and non-COVID ICU as well as axilla and groin swabs collected on all patients within both wards (n=22). One additional patient was identified with colonization from the axilla and groin swab, however, it was determined that this patient was not part of the outbreak due to differences in resistance patterns.

Each week thereafter the third (n=23) and fourth (n=16) point prevalence surveys were conducted on all patients within the COVID ICU and non-COVID ICU by collecting axilla and groin swabs and no additional patients were identified. A follow-up conference call was conducted with CDC experts and it was determined by expert consensus that two negative point prevalence surveys were sufficient evidence to stop conducting ASC and to monitor clinical specimens closely for 3 months. No environmental cultures were collected since fomite transmission was not suspected after two point prevalence surveys were conducted with no additional cases identified.

For each patient, a single BD BBL CultureSwab Plus (Becton Dickinson, Sparks, MD) swab was used to culture the axillae and the groin bilaterally, in that order. The specimens were inoculated within 1 hour of receipt in the Microbiology Laboratory to trypticase soy agar with 5% sheep blood (BAP), chocolate agar (CHOC), Columbia CNA agar (CNA), and MacConkey agar (MAC) plates (Becton Dickinson) and were incubated for 18-24 hours at 35°C in 5% CO 2 .

Culture plates were examined daily for 48 hours for colonies of growth meeting the morphologic criteria consistent with the genus Acinetobacter, and suspect colonies were identified to the species level by use of MALDI-TOF mass spectrometry (bioMerieux, Hazelwood, MO).

Antimicrobial susceptibility testing was performed on all isolates identified as Acinetobacter baumannii complex using the Vitek 2 (bioMerieux, Hazelwood, MO). Acinetobacter baumannii isolates that were defined as carbapenem-resistant were further tested in-house against minocycline and amikacin (Kirby Bauer), and ceftazidime/avibactam (ETEST), and submitted to ARUP Reference Laboratory (500 Chipeta Way, Salt Lake City, UT) for susceptibility testing against polymycin B and cefidericol. The isolates were also sent to the Tennessee Department of Health for confirmation of organism identification, and molecular testing of resistance genes KPC, NDM, OXA-48, VIM, IMP, OXA-42/40-like, OXA-58-like, and OXA-23-like. All isolates submitted were identified as having the molecular type OXA-23-like gene detected.

Acinetobacter baumanni has been found to survive on surfaces for months (Kramer et al., 2006 

Patient care interventions included increasing CHG bathing on all ICU patients to twice daily for patient decolonization. The respiratory therapists changed the ventilator circuits, tubing, suction and canister daily. Medication preparation practices that had been performed outside the patient room were moved back inside the room at the bedside on a clean bedside table.

Equipment that had been externalized was moved back inside the room. All supplies stored around the sinks were removed due to potential contamination risk. 

The manager of infection control identified patients on a line listing (Table 1) that was located in the COVID ICU due to acuity of illness. This patient's CRAB source was in the urine and then subsequently identified in the sputum. The fifth patient had been in the ICU since September 23, 2020 and initially hadF an MDRO Escherichia coli in the sputum before acquisition of CRAB. The sixth patient was identified through ASC in groin and axilla and later also grew CRAB in the sputum. There were 108 total screening specimens collected throughout the four point prevalence ASC. The rest of the containment strategies were in place for three months after the last point prevalence survey although PPE conservation was never reinstated in the ICU and targeted infection control rounds continued.

Patient care during the COVID-19 pandemic included a reversal of standard infection prevention and control containment strategies for MDROs. The first CRAB patient had multiple risk factors for MDRO and is believed to be the initial source of the outbreak. PPE conservation strategies and lapses in infection control during pandemic surge was the potential cause of transmission. On March 10, 2020, the infection preventionists at our organization educated staff on limited re-use of N95 respirators in non-contact isolation patients. Isolation gowns were not to be re-used for any suspected persons under investigation or positive COVID patients. PPE in our organization was highly controlled and continuously tracked utilizing burn rate calculators that predicted community surge and the supply needs of the healthcare system. On March 25, 2020, the CDC presented a COCA call describing best practices for optimization strategies for healthcare personnel PPE (Furuno et al., 2008) . Infection preventionists, supply chain, and administration continuously monitored the need for implementation of PPE conservation. The CDC guidelines for crisis capacity contingency strategies included "extending the use of isolation gowns such that the same gown is worn by the same provider when interacting with more than one patient housed in the same location and known to be infected with the same infectious disease (i.e., COVID-19 patients residing in an isolation cohort)" (CDC, 2019a).

Following this guidance, once an MDRO patient was identified, the gown conservation was to be immediately ceased. However, nosocomial transmission may have occurred prior to laboratory identification of an MDRO specimen when gown conservation was still in place. Furthermore, long length of stay of COVID patients, secondary infections, and the increased usage of antimicrobial agents in critically ill COVID patients may have contributed to MDRO formation through antibiotic pressure.

In order to decrease exposure to COVID, healthcare personnel began performing medication preparation outside of patient rooms prior to entry. Additionally, equipment such as However, modifying screening protocols could make ASC an effective tool and MDRO prevention strategy which included screening multiple body sites. A single swab test has only been found to be up to 30% sensitive in detecting A. baumannii (Marchaim et al., 2007) . New methods, including using a sponge to sample two sites simultaneously, have been found to be more than 80% sensitive in detection . Including both a swab of the buccal mucosa and sponge sample of the skin has been found to be the most effective with 99% sensitivity in CRAB detection (Nutman et al., 2020) . CDC partners also suggested using skin swabs for the point prevalence studies. High-risk patient settings or populations in areas with endemic MDROs could consider updating their ASC protocol with more sensitive methods and apply these methods to each patient admission. This screening effort should involve active participation from the laboratory to ensure that medical staff, infection control, and administration are immediately notified when an MDRO is identified. Finally, the importance of antimicrobial stewardship is evident and needed to suppress the emergence and spread of MDROs.

The first highly resistant CRAB specimen was detected in a sputum culture on a COVID- 

Epidemic curve of CRAB outbreak in COVID ICU. Tables   Table 1 Line listing of a CRAB outbreak in COVID ICU. 

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