key: cord-1040142-4j4dubdo
authors: Gao, Catherine A.; Bailey, Joseph I.; Walter, James M.; Coleman, John M.; Malsin, Elizabeth S.; Argento, A. Christine; Prickett, Michelle H.; Wunderink, Richard G.
title: Bronchoscopy on Intubated Patients with COVID-19 Is Associated with Low Infectious Risk to Operators
date: 2021-03-30
journal: Annals of the American Thoracic Society
DOI: 10.1513/annalsats.202009-1225rl
sha: cc92756b668b03617bdeb572f7aa0b31ed49cef6
doc_id: 1040142
cord_uid: 4j4dubdo

nan

Bacterial coinfections in viral pneumonia are well described and are associated with significant mortality (1) . Preliminary coronavirus disease 2019 (COVID-19) studies report bacterial coinfection (2), with higher rates associated with fatal outcomes (3) . Appropriate treatment of bacterial coinfection may therefore improve outcomes (4) . Accurate diagnosis of bacterial superinfection in ventilated patients with COVID-19 is important for appropriate antibiotic stewardship (5, 6) .

Bronchoalveolar lavage (BAL) with quantitative cultures is helpful (7) and is the standard in our intensive care unit (ICU) for both clinical and research purposes (2, 8) . Endotracheal aspirates have been shown to be inferior to BAL (9, 10) , involve a break in the closed ventilator circuit, and induce cough (11, 12) . Nonbronchoscopic BAL has similar aerosol-generating potential. We therefore shifted to a safety-modified bronchoscopic BAL technique for suspected COVID-19 pneumonia in our institution.

Concern that bronchoscopy exposes healthcare workers by generating aerosols (13) prompted professional society guidelines to discourage bronchoscopy in patients with COVID-19. However, this recommendation was based only on expert opinion (14, 15) , with a paucity of data. In a single-center report, one of two bronchoscopists developed COVID-19 and had to be replaced by a third, who remained uninfected for the duration of the study (16) . Other studies mentioned low provider infection rates, though details are not provided (17) .

Given our high volume of COVID-19 BALs (greater than 450 to date) on more than 280 ventilated patients with COVID-19, we designed the following study to assess the incidence of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection and seropositivity among bronchoscopists. Other studies from our institution (2, 18) show the typical patient being a male in his 60s; in our study comparing nasopharyngeal (NP) and BAL samples once intubated, the median duration between samples was 1 day (interquartile range [IQR], 1-2.75 d), demonstrating most patients underwent bronchoscopy early in their course. From these other studies, participants had an average of 1.63 BAL (range, 1-9) samples collected.

We surveyed all clinical faculty and fellows in our Pulmonary and Critical Care Division from July 30, 2020, to August 14, 2020 (survey available on request). Participants estimated the number of COVID-19 BALs that they performed, the number of weeks caring for ICU patients with COVID-19, and the results of any personal SARS-CoV-2 testing from March until August 14th. Participants assessed the difficulty of COVID-19 BALs compared with routine ICU BALs using a score ranging from 1 (easier) to 10 (harder). COVID-19 exposures outside of work were also queried. No identifiers were collected, and all respondents were offered the choice to decline to participate. The Vice Dean of Education and our Program Director gave permission to survey trainees. This study was deemed exempt by our institutional review board (STU00213164).

SARS-CoV-2 testing. NP testing for SARS-CoV-2 by polymerase chain reaction (multiple platforms) was performed on providers at the discretion of our hospital's infection control team, either in response to symptoms, after a known exposure, or as routine preprocedure screening. Serology (Architect SARS-CoV IgG; Abbott) testing was offered to all medical staff by our hospital.

COVID-19 bronchoscopy protocol. The decision to perform bronchoscopy was at the discretion of the ICU team, and bronchoscopies were performed by pulmonary critical care attendings and/or pulmonary/interventional pulmonary fellows. Our typical practice was to perform bronchoscopy on intubation while the patient remained neuromuscularly paralyzed from induction to confirm or rule out COVID-19 infection and to evaluate for any bacterial coinfection. Repeat bronchoscopies were performed as clinically indicated in response to concern for infection or otherwise at the discretion of the ICU team.

The full modified protocol is available online (19) . Nurses and respiratory therapists were not in the rooms during the actual bronchoscopy. Personal protective equipment (PPE) included an N95 mask, eye protection, gloves, gown, and hair protection. Bronchoscopy was performed with a disposable Ambu aScope (Ambu, Inc.) bronchoscope. Patients were sedated per ICU protocols or at the proceduralist's discretion. Administration of cisatracurium (0.1-0.2 mg/kg) to minimize coughing during bronchoscopy was recommended. The endotracheal tube was clamped, and the inspiratory limb of the ventilator was transiently disconnected while the ventilator circuit was manipulated to accommodate scope placement.

The protocol was developed early in the pandemic by a multidisciplinary team and distributed to bronchoscopists online, through e-mail, and within the hospital's COVID-19 ICU protocols manual. Although protocol adherence was not specifically monitored, most of the providers were taught the protocol by our interventional pulmonary faculty, who also performed a large number of the bronchoscopies.

Statistical analyses. Not all continuous data were normally distributed, and so median values with IQRs were reported. Nonparametric analyses included Mann-Whitney U test and Spearman's rank correlation for continuous variables. Kruskal-Wallis rank testing was used to compare values across multiple categories. 

Forty-five of 52 clinical pulmonary and critical care faculty and fellows agreed to participate (90% response rate), including 18 fellows and 27 faculty members ( Table 1 ). The majority (35/45; 78%) performed at least one COVID-19 BAL, with most respondents performing between 10 and 30.

Of respondents, 42% spent more than 5 weeks on a COVID-19 ICU service. The number of weeks on COVID-19 ICU service correlated with bronchoscopy volume (Spearman r 5 0.66; P , 0.05). The overall median perceived difficulty score was 6 (6-7) and did not correlate with amount of training, bronchoscopy volume, or time spent on ICU service with patients with COVID-19 (P . 0.05). Two respondents reported performing bronchoscopy without full PPE under emergent situations, and 12 reported performing bronchoscopies without following the full protocol.

Of all respondents, 18/45 (40%) had NP testing, and 36/45 (80%) had serology testing. Of the subset of 35 providers performing COVID-19 BALs, 16/35 (46%) underwent at least one NP swab for SARS-CoV-2; five had a respiratory illness that prompted their testing, and eight were tested for screening purposes. No respondent reported a positive test. SARS-CoV-2 serology was negative on all but one of the 27/35 (77%) bronchoscopists tested. This individual had two sets (one positive, the second negative). This individual spent more than 5 weeks on a COVID-19 ICU service and performed 10-30 bronchoscopies but had no febrile respiratory symptoms.

Our data represent the first detailed report of infectious risks to providers from a large-volume center that routinely incorporates BAL as part of critical care for patients with and without COVID-19 respiratory failure. We hypothesized that careful bronchoscopy technique can limit infectious risk. Although limited to a single center, our data suggest that the risk of transmitting COVID-19 to providers performing BAL is low. No provider developed COVID-19, and only one had positive serology. Our cohort's seropositivity rate was actually lower than what was found among all healthcare workers at our institution (4.8%), although they also found that bronchoscopy was not associated with increased seropositive rates (20) .

Our group supports adherence to evidence-based critical care during the COVID-19 pandemic (21) . Professional society guidelines cautioning against bronchoscopy for patients with COVID-19 (14, 15) are only based on expert opinion. Initial concerns about the safety of bronchoscopy in patients with COVID-19 overestimate the risk of provider infection, and our results are reassuring to the bronchoscopist community.

This survey was not a formal study of our specific bronchoscopy protocol. However, we hypothesized that careful technique during bronchoscopy can limit infectious risk. Principles of our protocol included 1) limiting the number of providers in the room, 2) minimizing aerosol generation by with clamping the endotracheal tube and disconnecting the inspiratory limb of the ventilator during manipulations, 3) minimizing cough by neuromuscular blockade or heavy sedation and instillation of lidocaine into the tracheobronchial tree, and 4) use of a disposable bronchoscope. We also had a small number of highly skilled providers (our interventional pulmonary team) performing a high number of the BALs. The interventional pulmonary team volunteered during the pandemic to provide this service for a variety of reasons, including the high workload of primary attending pulmonary critical care faculty/fellows, increased health risk of some fellows and faculty, and coverage by non-pulmonary critical care medicine staff and fellows for some cases. We worried that the increased number of steps, attention to special points, and burden of PPE would increase procedure difficulty for providers. Fortunately, most providers believed that the bronchoscopies following the protocol were only slightly more difficult than routine ICU bronchoscopy, given the increased number of steps, greater care to avoid circuit breaks, fewer providers, and increased amount of PPE. We suspect that other centers may have similar protocols, and a more scientific exploration of techniques would be needed to comment on protocol efficacy compared with standard procedure with just additional PPE.

Our study has limitations. First, this is a retrospective survey of providers and their recollection. Electronic medical records were not monitored to respect our colleagues' privacy, but we instead used voluntary responses. Bronchoscopy protocol adherence was not monitored explicitly, and some operators reported less than complete compliance. Although we were unable to capture a 100% response rate, our results are higher than most physician survey response rates (22) . Despite testing being offered to all providers, only a subset was actually tested, and our results may therefore underrepresent the true infectious risk; it is also possible that asymptomatic infections were missed if providers did not seek testing in a short time period after performing COVID-19 BALs. We also did not gather specific time points of testing and cannot correlate test results directly relative to when BAL was performed and how far in the patients' time course the BAL was done (infectivity may wane over time, although many BALs were performed upon intubation, during which infectivity would be hypothesized to be high). Some of our institution's bronchoscopy timing can be viewed in the results of other manuscripts on part of our patient cohort (2). Our results may not be generalizable to centers that do not routinely perform BAL in critically ill intubated patients. In summary, although additional research is needed to inform optimal use of BAL to improve outcomes for ventilated patients with COVID-19, our data suggest that careful, protocolled BAL routinely incorporated into COVID-19 ICU care offers minimal infectious risk to providers.

Radhika Patel

Increased incidence of co-infection in critically ill patients with influenza

Alveolitis in severe SARS-CoV-2 pneumonia is driven by self-sustaining circuits between infected alveolar macrophages and T cells

Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study

Co-infections: potentially lethal and unexplored in COVID-19

Principles and practice of antibiotic stewardship in the ICU

Stewardship in the intensive care unit: an official american thoracic society workshop report in collaboration with the AACN, CHEST

International ERS/ESICM/ESCMID/ALAT guidelines for the management of hospital-acquired pneumonia and ventilatorassociated pneumonia: guidelines for the management of hospitalacquired pneumonia (HAP)/ventilator-associated pneumonia (VAP) of the

Multidimensional assessment of alveolar T cells in critically ill patients

Invasive and noninvasive strategies for management of suspected ventilator-associated pneumonia: a randomized trial

Comparison of semi-quantitative endotracheal aspirates to quantitative non-bronchoscopic bronchoalveolar lavage in diagnosing ventilator-associated pneumonia

Invasive and non-invasive diagnostic approaches for microbiological diagnosis of hospital-acquired pneumonia

Quantitative cultures of endotracheal aspirates for the diagnosis of ventilator-associated pneumonia

Aerosol generating procedures and risk of transmission of acute respiratory infections to healthcare workers: a systematic review

American Association for Bronchology and Interventional Pulmonology (AABIP) statement on the use of bronchoscopy and respiratory specimen collection in patients with suspected or confirmed COVID-19 infection

The use of bronchoscopy during the coronavirus disease 2019 pandemic: CHEST/AABIP guideline and expert panel report

Bronchoscopy in patients with COVID-19 with invasive mechanical ventilation: a single-center experience

Extracorporeal membrane oxygenation support in severe COVID

Comparing nasopharyngeal and BAL SARS-CoV-2 assays in respiratory failure

Northwestern Medicine. NMH COVID ICU guidelines

Seroprevalence and correlates of SARS-CoV-2 antibodies in health care workers in Chicago

A call for rational intensive care in the era of COVID-19

Physician response to surveys: a review of the literature

BRR centers are specialized in bronchiectasis care, and population-based data bronchiectasis (4, 7), but the validity of using Medicare claims to identify P. aeruginosa infection is unknown. Accordingly, we validated Medicare claims using the BRR as a gold standard. We identified patients with a bronchiectasis diagnosis (International Classification of Diseases, Ninth Revision, Clinical Modification

The Medicare observation period began on the later date of enrollment or data start

The BRR observation started 24 months before enrollment and ended at loss to follow-up. Linked patients with an overlap between BRR and Medicare observation were examined

outpatient ICD-9-CM claims for P. aeruginosa infection and excluding claims and cultures outside this overlap.We explored the primary case definition of ICD-9-CM code 482.1 (Pseudomonas pneumonia) given by a clinician as well as alternate definitions using codes 482.1 and/or 041.7 (Pseudomonas, unspecified site). "True" cases of P. aeruginosa infection were identified on the basis of culture positivity in the BRR. We