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Journal of Bronchology & Interventional Pulmonology:
doi: 10.1097/LBR.0000000000000075
Original Investigations

Impact of Bedside Bronchoscopy in Critically Ill Lung Transplant Recipients

Mohanka, Manish R. MD, MPH*; Mehta, Atul C. MD; Budev, Marie M. DO, MPH; Machuzak, Michael S. MD; Gildea, Thomas R. MD, MS

Free Access
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Author Information

*University of Texas Southwestern Medical Center, Dallas, TX

Cleveland Clinic Foundation, Cleveland, OH

Disclosure: There is no conflict of interest or other disclosures.

Reprints: Manish R. Mohanka, MD, MPH, University of Texas Southwestern Medical Center, 5939 Harry Hines Blvd., HQ1.200, Dallas, TX 75390-8550 (e-mail: manish.mohanka@utsouthwestern.edu).

Received July 21, 2013

Accepted April 14, 2014

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Abstract

Background: Over 32,000 lung transplants have been performed worldwide for a variety of end-stage lung diseases (http://www.ishlt.org/). Flexible bronchoscopy (FB) is frequently used as a bedside-tool for diagnosis and management of respiratory failure among critically ill lung transplant recipients (LTRs). We study the indications, results, therapeutic impact, and complications of FB in LTRs admitted to medical intensive care unit (MICU).

Methods: Retrospective chart review was performed for all critically ill LTRs undergoing FB while admitted to MICU at the Cleveland Clinic Foundation between 2009 and 2011. ICD-9 codes for bronchoscopy were used to identify patients. The procedures were categorized as: (i) airway examination and interventions, (ii) microbiological, and (iii) histopathologic diagnosis. SAS version 9.2 was used for analysis.

Results: A cohort of 76 LTRs accounted for 93 hospital admissions, 101 MICU admissions, and 129 bronchoscopies. FB was helpful in evaluation and management of airway complications [secretion clearance (18% bronchoscopy procedures), stenosis/dehiscence (8% patients)] and optimizing management of lower respiratory tract infections. Isolation of resistant gram-negative organisms, community-acquired respiratory viruses, and fungi commonly led to modification in antimicrobial therapy (35% microbiological samples). Nonspecific finding of acute lung injury was the most commonly seen histopathology (70%) on transbronchial biopsy. Twenty percent (4/20) of transbronchial biopsies showed acute cellular rejection, with 1 episode contributing to respiratory failure. Occasional hypoxia and hypotension, but no deaths, were noted due to FB during the ICU admission.

Conclusions: Use of FB modified clinical management in one third of airway evaluation and microbiological sampling procedures for critically ill LTRs. No fatalities were attributed to bronchoscopy in this critically ill population.

More than 32,000 lung transplants have been performed worldwide for a variety of end-stage lung diseases and over 3000 lung transplants are performed annually around the world (http://www.ishlt.org/). Following transplantation, many serious complications occur, leading to the admission of transplant patients to the intensive care unit (ICU). Previous small single-center studies have demonstrated that a sizeable percentage (17% to 23%) of lung transplant recipients (LTR) require ICU admission.1–4 Major causes for these ICU admissions were sepsis and respiratory failure. Management of LTRs is challenging,5 especially when critically ill. Flexible bronchoscopy (FB), a frequently used bedside diagnostic and therapeutic tool among critically ill patients, is associated with pathophysiological impact including respiratory, cardiovascular, and other systemic derangements.6,7

The primary goal of this study was to describe the utility of bedside FB among critically ill LTRs. We describe the indications, various diagnostic and therapeutic techniques used, results thereof, and procedure-related complications. We categorized the procedures as: (i) airway examination and airway interventions, (ii) microbiological, and (iii) histopathologic sampling procedures.

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PATIENTS AND METHODS

We conducted a retrospective chart review of all LTRs who underwent FB while admitted to the medical intensive care unit (MICU) at a large lung transplant institution between January 1, 2009 and December 31, 2011. Patients were identified using ICD-9 codes for bronchoscopy and data were extracted without personal identifiers from electronic medical records. Study was approved by the institutional review board at the Cleveland Clinic (IRB#12-191).

The standard practice at our institution is to care for the LTRs in the cardiothoracic ICU in early postoperative period followed by transfer to transplant floor units. If patients need readmission to the ICU, they are admitted to MICU, unless the indication is primarily surgical. Our study only includes critically ill LTRs in the MICU.

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Data Collection

We collected the demographic and transplant data, chest radiology findings, various diagnostic and therapeutic procedures performed during FB (including microbiological, histopathologic sampling), complications, and the subsequent impact on patient management. The primary diagnosis for MICU admission was noted. For bronchoscopy, all documented indications were noted and chest imaging findings on radiology reports were confirmed by the primary investigator. Nonspecific finding of atelectasis versus infiltrate was defaulted to infiltrate.

In our study, airway problems (ie, bronchial stenosis) were documented only when considered clinically significant for causing symptoms, or needing intervention. When bronchoalveolar lavage (BAL) was attempted but not successfully completed, the procedure was documented as bronchial wash. Single-protected brush specimen was combined with results of BAL. Empiric antibiotics administered until the day of bronchoscopy was recorded. Availability of fluoroscopy for transbronchial biopsies (TBBX) was noted. Complications were documented as an outcome only when these invited specific management (eg, vasopressor medications for hypotension) or resulted in termination of procedure.

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Statistical Analysis

SAS version 9.2 (Cary, NC) was used. Descriptive analysis was performed for findings of airway examination, interventional procedures, and diagnostic procedures. For diagnostic microbiology and histopathology sampling, we evaluated predictors of results that led to change in therapy [eg, isolation of resistant microorganisms, acute cellular rejection (ACR), etc]. Multivariate analysis was performed for microbiological sampling using multiple logistic regression models with backward variable selection procedure.

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RESULTS

Seventy-six LTRs accounted for 93 hospital admissions, 101 MICU admissions, and 129 bronchoscopies. Demographics, pretransplant diagnoses, and primary diagnosis for MICU admission are presented in Table 1. Respiratory failure (hypoxic or hypercapneic), and sepsis/hypotension were the most common reasons for MICU admission. Evaluation for lung infiltrates on chest imaging, such as chest x-ray or computed tomography, was an indication in 68% of procedures (Table 2).

Table 1
Table 1
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Table 2
Table 2
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Airway Examination and Airway Intervention

The most common reason for isolated airway examination was suspected atelectasis (Table 3). Retained secretions or blood was found upon bronchoscopy in the vast majority. The median duration from lung transplant to bronchoscopy for therapeutic aspiration was 6 months. The paO2/FiO2 ratio improved after 65% of procedures with geometric mean improvement of 30%. Chest imaging showed improved aeration after 41% procedures.

Table 3
Table 3
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Airway evaluation for stenosis resulted in finding clinically significant abnormality not documented on earlier bronchoscopies, about one third of the time. These were suspected for hypercapneic respiratory failure and difficulty weaning off mechanical ventilation. Both anastomotic dehiscence were incidentally discovered during microbiological sampling for clinical sepsis/hypoxia associated with infiltrates on chest imaging. There was no evidence of pneumothorax on chest imaging. They were discovered at 6 weeks and 11 months. One patient needed airway stent, whereas the other was managed conservatively due to very small area of dehiscence. Bronchoscopy identified source of hemoptysis to tracheostomy site in 3/6 patients. Bronchoscopy was also used to secure endotracheal intubation (4 patients), including a patient with subglottic-stenosis and for selective lung intubation with hemoptysis in another.

Six patients (stenosis 4, dehiscence 2) with airway abnormalities required 12 interventional pulmonary procedures. A variety of airway ablation, dilation, stenting, and topical medication application (eg, mitomycin) procedures were performed with concurrent use of rigid bronchoscopy.

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Microbiological Evaluation

Ninety-nine microbiological specimens (79 BAL, 19 bronchial wash, and 1 protected brush specimen) were obtained through bronchoscopy, a median of 1 day (25th, 75th percentile: 0, 4 d) after MICU admission (Table 4). We obtained the BAL sample with instillation of three 20 mL aliquots of sterile normal saline from the abnormal-appearing area on chest imaging. Infiltrates on chest imaging and/or purulent respiratory secretions were present in all patients. Ninety-six percent patients received empiric antibiotics for a median of 3 days (1, 10 d) before bronchoscopy, covering gram-positive (91%), gram-negative (96%), atypical (50%), fungal (45%), and viral (42%) organisms. Isolated microorganisms are presented in Table 4.

Table 4
Table 4
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Pseudomonas aeruginosa was the most commonly isolated of all organisms. Eighty percent of gram-negative bacilli (GNB) were isolated after 5 days (mean 36±43 d) of hospital stay. The GNB coverage of empiric antibiotics was inadequate in 50% (9/18) instances, mostly (n=8) due to antimicrobial resistance patterns. In most other instances, results were helpful in tailoring the antimicrobial regimen or duration. Gram-positive bacteria were covered by empiric antibiotics in the majority of cases, except when vancomycin-resistant enterococci were isolated and needed further tailoring of antibiotic therapy.

Cytomegalovirus (CMV) was the most commonly isolated virus, and was already being treated in 3/6 instances for viremia. Three of the 6 patients were CMV mismatch (donor+/recipient−). One patient with CMV pneumonitis had alveolar hemorrhage on BAL. Community-acquired respiratory viruses (CARV) isolated were treated (n=5) with specific antiviral therapy with or without intravenous immunoglobulin.

Among the fungi, Candida albicans was isolated on 6 occasions, and treated on 4 instances; the other cases were not felt to be contributing to the clinical presentation. Other species of Candida, Aspergillus, positive BAL Galactomannan testing, as well as “non-candida, non-cryptococcus yeast not identified further” also resulted in systemic treatment.

Overall, microbiological results from 35% bronchoscopies helped optimize regimen and/or duration of antibiotics. Fifty-eight isolates of pathologic microorganisms were found, and the empiric antibiotic therapy was inadequate for at least 25 of these instances either due to inadequate initial coverage or antibiotic resistance patterns (mostly GNBs).

On univariate analysis, MICU admission diagnosis of sepsis (OR=6.4, Fischer exact test), absolute WBC count on BAL (per 100 U increase), percent-neutrophil count on BAL fluid, and percent-neutrophil count on complete blood counts on bronchoscopy day (all P<0.05, Wilcoxon rank-sum test) were associated with subsequent isolation of pathogenic microorganism. On multivariate analysis, only MICU admission diagnosis of sepsis (OR=4.06; 95% CI, 1.12-14.68, P=0.033) and high WBC count in BAL (OR=1.08; 95% CI, 1.01-1.15, P=0.020) predicted subsequent isolation of pathogenic microorganism. For unclear reasons, hypoxia on MICU admission was inversely associated on univariate analysis, but this association was not observed in multivariate analysis (OR=0.69, Fischer exact test). Other independent variables tested included age, pretransplant diagnosis, single versus bilateral lung transplant, time since transplant, fever, respiratory failure, lung infiltrate, sputum characteristics, empiric antibiotic use, airway stents, degree of hypoxia (paO2/FiO2 and PEEP), immunosuppressive regimen, IgG level, and procalcitonin levels.

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Transbronchial Biopsies (TBBX)

Eighteen patients underwent 20 TBBX 195±190 days posttransplant and 2.9±3.1 days after MICU admission. Hypoxemia and transplant-lung infiltrates on chest imaging were observed in all patients. Eighteen procedures were performed during mechanical ventilation support and fluoroscopy was available for 8 procedures. Diagnostic tissue to evaluate for ACR was not obtained during 5 procedures.

The most common histopathologic finding was acute lung injury (ALI)/inflammation (Fig. 1). ACR was discovered on 4 procedures [3 minimal (A1), 1 mild (A2)], all within the first posttransplant year. A2 rejection was felt to contribute to respiratory failure and was treated with pulsed corticosteroids. A1 was managed with augmented immunosuppression including steroids and calcineurin inhibitors. All C3D/C4D tests (n=12) were negative, 2 others were nondiagnostic. ALI was commonly associated with pneumonia. None of the hypothesized variables predicted finding ACR on TBBX on univariate analysis. These included pretransplant diagnosis, time since transplant, immunosuppression regimen, prior number of ACR, and BAL WBC count.

Figure 1
Figure 1
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Survival and Length of Hospital Stay

Thirty-three inpatient deaths occurred among 76 LTRs during 93 hospitalizations (35.4% mortality). Two of the 3 patients transferred to hospice for terminal care had bronchiolitis obliterans syndrome. One other patient had squamous cell cancer of head and neck. When bronchoscopy was used for microbiological sampling, isolation of a microbiological agent did not impact (all P=NS, t test) the MICU (16±14 vs. 11±9) or hospital length-of-stay (31±26 vs. 53±45 d), or the survival of patient on hospital discharge (34% vs. 44%). These were also not different whether or not the empiric antibiotic adequately covered the isolated microorganism.

When discharged alive, 6 patients were transferred to long-term acute care facility for severe debility and 2 required inpatient physical rehabilitation.

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Major Complications of Bronchoscopy

Hypoxia (n=4, 3%) and hypotension (n=4, 3%) of significant degree were the most common complications. Two of them required transient vasopressor support. Pneumothorax (n=1) and airway bleeding (n=1) were encountered after TBBX. Pneumothorax was observed after TBBX performed on mechanical ventilation support despite fluoroscopy use, and required chest tube placement. Airway bleeding was controlled with cold saline instillation. One patient suffered small airway tear during balloon dilation for bronchial stenosis, needing an airway stent. Two instances of supraventricular arrhythmia were noted, both in the same patient, which required electrical and chemical cardioversion. Both procedures were aborted. No deaths were directly attributable to bronchoscopy.

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DISCUSSION

Airway Examination

Impaired secretion clearance among LTRs is related to the presence of anastomosis, mucosal ischemia, decreased ciliary beat frequency,8,9 loss of innervation with impaired cough,10 and/or immunosuppression.11 It can persist beyond the first posttransplant year.11,12 The improvement in oxygenation and chest imaging with therapeutic aspiration observed is comparable with prior studies among other populations.13 Among non-LTRs, bronchoscopy is suggested for patients remaining symptomatic after 24 hours of aggressive chest physiotherapy.14,15 Albuterol can enhance mucociliary clearance among LTRs.11

Our rates of airway complications were lower than prior studies (7.8% vs. 8.3% to 20%), partly because of our stringent study outcomes criteria.16–18 Prior publications from our institution have described management approaches for airway complications.19–21 Use of airway stents for significant stenosis among LTRs can improve FEV1,18 symptoms, and achieve permanent patency among the vast majority.16 Patients in our study were transferred to lower level-of-care between 1 and 8 days after the initial airway intervention. Early liberation from mechanical ventilation and change in the level-of-care after airway intervention has been reported for benign and malignant central airway obstruction.22

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Microbiological Evaluation

Pneumonia is the most common infection after lung and heart-lung transplantation.23–25 When clinically suspected, microbiological sampling by bronchoscopy modified antimicrobial management in about 35% cases in our study, mostly related to isolation of resistant gram-negative bacteria, non-CMV respiratory viruses, and fungi. Mattner et al23 described P. aeruginosa, Staphylococcus aureus, and other GNB as the most common pathogens for pneumonia among heart and heart-lung recipients routinely admitted to ICU between 2 and 250 days posttransplant. Similar spectrum has been described among noncritically ill LTRs during clinically indicated bronchoscopies.24–28

CMV was the most common virus isolated in our study. Before availability of effective oral antiviral prophylaxis, CMV pneumonitis was reported in 4% to 10% and CMV infection (isolation of CMV in BAL) in over 20% of clinically indicated bronchoscopies among noncritically ill LTRs.26,27 Lower rates of infection in our study (1% pneumonitis, 6% infection) likely reflects use of prophylactic valganciclovir in at-risk patients.29,30

The spectrum of CARV in our study was conspicuous by the absence of rhinovirus and coronavirus, commonly isolated during surveillance bronchoscopies.31–34

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Fungal

We routinely give prophylaxis with inhaled amphotericin B (early postoperatively) and oral itraconazole with close monitoring of levels. When Aspergillus was isolated, there was no clinical evidence of dissemination in our study.35,36 C. albicans was the most commonly isolated fungus in our study, and treated with systemic agents due to concerns for the health of surgical anastomosis.37 Mortality and hospital length-of-stay in the group where a specific microorganism was isolated was not different compared with other patients. Nearly all patients received empiric antibiotic therapy and it is plausible that only the resistant microbes were isolated. MICU admission diagnosis of sepsis/hypotension with suspected pneumonia, and elevated WBC count in BAL/bronchial washings may predict subsequent isolation of pathogen.

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Histopathologic Evaluation

ALI is a nonspecific finding, and may be seen with infections and antibody-mediated rejection. Overall, we found 20% yield of TBBX with minimal-mild (A1-A2) ACR, all within the first-year posttransplantation. A prior study38 reported overall 37% diagnostic yield of performing TBBX, with 11% ACR. The higher yield in this study was driven by finding of 26% infections. The diagnostic utility of clinically indicated TBBX among noncritically ill adult and pediatric LTRs has been reported in the range 26% to 65%26,27 and 54%,39 respectively. Diagnoses range from ACR, lymphocytic bronchiolitis, and infection.

TBBX when compared with surgical lung biopsy (gold standard) among critically ill, mechanically ventilated LTRs carries poor sensitivity to diagnose ACR (53% sensitivity), especially grade ≥A2a (36%).40 It also tends to underestimate the grade of ACR. At our institution, we obtain TBBX from 2 different lobes on the same side, collecting 6 to 8 pieces of tissue. This may improve the sensitivity of TBBX for detecting ACR. When on mechanical ventilation, TBBX are performed by experienced bronchoscopists. We allow for adequate sedation to minimize patient discomfort and movement, reduce PEEP below 5 and preferably to 0, whenever tolerated. To minimize airway bleeding after TBBX, we wedge the bronchoscope in position for 4 minutes. Fluoroscopic guidance is not available in our ICU, but may be used when the patient is transferred to bronchoscopy suite (40% TBBX).

As finding of ACR on TBBX is specific, any grade of ACR noted should be treated with augmented immunosuppression. Because of low sensitivity of TBBX, it cannot rule out ACR and should be treated as such when clinically suspected.

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Complications

Hypoxia and hypotension were the most common complications. There were no associated fatalities. Pneumothorax was noted on 1 occasion (5.5%) despite fluoroscopy use in mechanically ventilated patient. Prior studies among mechanically ventilated LTRs have reported rates between 2.3% and 6.5%.38,40 Lower pneumothorax rates among mechanically ventilated LTRs compared with non-LTRs (6.6% to 23%)38,41–44 may be related to pleural adhesions among LTRs, differences in experience, techniques, and/or facilities at lung transplant programs. Rates of pneumothorax among nonmechanically ventilated LTRs are lower (1.5%).27

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Strengths of Our Study

This is the first study to comprehensively evaluate the utility of all bronchoscopic procedures among critically ill LTRs. Our data comprises all bronchoscopies serially performed over the 3-year duration and thereby reflects usual practices in MICU from a high-volume lung transplant center. It can provide an insight into expected outcomes from bedside bronchoscopy and aid clinical decision making.

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Weaknesses of Our Study

First, this study is a retrospective cohort design without a control group. Therefore we cannot compare the performance of FB with other techniques; for example, BAL versus noninvasive microbiological sampling. Early bronchoscopy may also reduce the drive for alternative noninvasive techniques. The benefits and risks of bronchoscopy versus other diagnostic and therapeutic techniques will need to be validated in future comparative studies.

Second, for microbiological sampling, the actual timing of empiric antibiotic administration (before/after bronchoscopy) could not be ascertained for all patients. Therefore we recorded antibiotics administered until the date of bronchoscopy and this may have introduced bias. However, reanalyzing the data with antibiotics administered till the day before bronchoscopy did not change our results.

Third, this study reflects practices in a high-volume lung transplant center. Although most lung transplant centers are well-equipped hospitals, availability, practices, and threshold for performing testing such as FB would likely be different in different settings.

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CONCLUSIONS

Use of bedside bronchoscopy modified patient management in one third of airway evaluation and microbiological sampling procedures. The yield of performing transbronchial biopsy was modest. No fatalities were attributed to performing bronchoscopy among critically ill LTRs. Further studies are warranted to evaluate performance of bronchoscopy compared with less-invasive diagnostic tests, especially for microbiological sampling.

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Keywords:

lung transplantation; bronchoscopy; critical care medicine; opportunistic infections

© 2014 by Lippincott Williams & Wilkins.

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