Halawa ARR, Farooq S, Amjad MA, Jani PP, Cherian SV. Role of interventional pulmonology in intensive care units: A scoping review. World J Crit Care Med 2025; 14(2): 99654 [DOI: 10.5492/wjccm.v14.i2.99654]
Corresponding Author of This Article
Sujith V Cherian, FCCP, MBBS, MD, Associate Professor, Department of Critical Care, Pulmonary and Sleep Medicine, University of Texas Health-McGovern Medical School, 6431 Fannin Street, Houston, TX 77030, United States. sujith.v.cherian@uth.tmc.edu
Research Domain of This Article
Respiratory System
Article-Type of This Article
Minireviews
Open-Access Policy of This Article
This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Abdul Rahman R Halawa, Saad Farooq, Mohammad Asim Amjad, Pushan P Jani, Sujith V Cherian, Department of Critical Care, Pulmonary and Sleep Medicine, University of Texas Health-McGovern Medical School, Houston, TX 77030, United States
Author contributions: Halawa ARR, Farooq S, Amjad MA, and Cherian SV were responsible for conception and design; Jani PP and Cherian SV were responsible for administrative support and provision of study materials or patients; Halawa ARR, Farooq S, and Amjad MA were responsible for collection and assembly of data and data analysis and interpretation; Halawa ARR, Farooq S, Amjad MA, Jani PP, and Cherian SV were responsible for manuscript writing; all of the authors read and approved the final version of the manuscript to be published.
Conflict-of-interest statement: There are no conflicts of interest.
Open Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Sujith V Cherian, FCCP, MBBS, MD, Associate Professor, Department of Critical Care, Pulmonary and Sleep Medicine, University of Texas Health-McGovern Medical School, 6431 Fannin Street, Houston, TX 77030, United States. sujith.v.cherian@uth.tmc.edu
Received: July 27, 2024 Revised: October 31, 2024 Accepted: December 23, 2024 Published online: June 9, 2025 Processing time: 215 Days and 5.4 Hours
Abstract
Interventional pulmonology (IP) represents a rapidly growing and developing subspecialty within pulmonary medicine. To the intensivist, given the elaborate undertakings with respect to airway, lung and pleural disease management-IP has shown an increasing presence and remain a major ally in the care of these patients. Thus, an understanding of the different roles that IP could offer to the intensivist is of prime importance in the multi-disciplinary care of the complex patients within the intensive care units, particularly in relation to lung, airway and pleural diseases. This review article will explore the different intersections of IP in critical care and discuss the applications of this discipline within the highly complex critical care environment.
Core Tip: The role of interventional pulmonology (IP) in critical care is described within this review article which will highlight the role of IP in the management of critically ill patients, particularly in patients with respiratory failure due to several reasons including hemoptysis, central airway obstruction and its different etiologies including malignancies, foreign body aspirations, blood clots and mucus. Moreover, the role of IP in management of pleural diseases, use of different tools such as endobronchial ultrasound in diagnosis of pulmonary vascular issues in the critically ill patient will be described. Finally, the role of IP in performing bedside procedures such as tracheostomy and percutaneous ultrasound gastrostomies with consequent economic benefits and decrease in lengths of stay will be outlined.
Citation: Halawa ARR, Farooq S, Amjad MA, Jani PP, Cherian SV. Role of interventional pulmonology in intensive care units: A scoping review. World J Crit Care Med 2025; 14(2): 99654
Interventional pulmonology (IP) procedures are indispensable in managing patients hospitalized in the intensive care unit (ICU). The applications of IP include but are not limited to patients with central airway obstruction (CAO), hemoptysis, and respiratory failure resulting from numerous causes such as foreign bodies, blood clots and mucoid impaction of airways. Various equipments in the interventional pulmonologist’s arsenal, including rigid bronchoscopy (Figure 1A), argon plasma coagulation (APC) and cryotherapy (Figure 1B) are of crucial importance while addressing these challenging cases. Moreover, pleural diseases are common in the critical care units and a structured approach to manage these conditions is of particular importance. The increasing utility of endobronchial ultrasonography in the ICU and its influence on clinical decision-making is gaining recognition. The decision to pursue tracheostomy is pertinent in patients who are faced with prolonged dependence on mechanical ventilation. Additionally, establishing nutritional access in the same setting through a gastrostomy tube is frequently required. Both procedures are being performed by interventional pulmonologists at the bedside. The purpose of this review article is to provide an outline of the different pathways and roles IP plays in the care of patients in critical care units.
Figure 1 Instrument.
A: Rigid bronchoscopy and its accessories–notice the different types of forceps with its larger sizes which are helpful in foreign body removal; B: ERBE combined argon plasma coagulation and cryotherapy machine.
HEMOPTYSIS
The expectoration of blood from the lower respiratory tract is referred to as hemoptysis. While unlikely to be associated with exsanguination and hemorrhagic shock, it may lead to respiratory failure due to ventilation/perfusion mismatch, or subsequent airway blockage. Hemoptysis, when leading to such respiratory complications is referred to as life-threatening hemoptysis. There is no precise quantitative parameter to define life-threatening hemoptysis, one criteria based on blood volume that has been suggested is approximately 150 mL in a 24-hour period or a bleeding rate that is greater than or equal to 100 mL/hour, which in layman terms would equate to half a cup of blood[1].
Blood supply to the lungs is composed of two sources, the pulmonary arteries and the bronchial arteries. The pulmonary artery circulation is a low-pressure system supplying the lung parenchyma, in contrast to the bronchial artery circulation which is a relatively high-pressure system supplying the bronchial tree, and 2% of the total vascular supply to the lung. In most cases of non-life-threatening hemoptysis, the origin is usually from the pulmonary artery circulation, compared to life-threatening hemoptysis, in which the source is more likely from a bronchial artery[2]. The most common causes of non-life-threatening hemoptysis in developed countries are acute bronchitis, bronchiectasis, pneumonia, lung cancer, and bronchial neoplasms[3]. Other noteworthy etiologies are autoimmune disorders such as anti-glomerular basement membrane, systemic lupus erythematosus, vasculitis, pulmonary embolism (PE), tuberculosis, and medications such as VEGF inhibitors[4]. Rare etiologies include pulmonary arteriovenous malformations, which may be seen in the setting of hereditary hemorrhagic telangiectasia, pulmonary artery aneurysms, and aorto-bronchial or broncho-pulmonary arterial fistulas. Furthermore, coagulopathy due to medications, renal failure, or liver disease can predispose to hemoptysis in patients with underlying lung pathology[4]. Despite a thorough workup, up to 30% of patients with hemoptysis may not have a cause identified, however, repeating work up when symptoms recur may yield a diagnosis[5].
Diagnosis
Management of patients with hemoptysis is centered around assessment of hemodynamic stability and respiratory compromise. In hemodynamically stable patients, a thorough history and physical should be obtained, in addition to imaging of the chest. Determination of the frequency and severity of bleeding is of utmost importance. It is crucial to ascertain if there is true airway bleeding or a potential mimicker such as hematemesis. Clues on physical exam that may point towards pseudo-hemoptysis include stigmata of liver disease, visualization of hematemesis, blood-tinged nasal crusting, and nasopharyngeal or mucosal ulceration. Laboratory studies such as hemoglobin, platelet count, liver function tests and coagulation profile should be collected. Even though hemoglobin may be normal in the acute setting, airway bleeding leads to mortality secondary to asphyxiation rather than blood loss, therefore clinicians should be vigilant in cases of hemoptysis. As mentioned above, as little as 150 cc of blood would be enough to occlude the airways.
Management
In cases of hemodynamic instability or respiratory failure, endotracheal intubation should be contemplated to ensure airway security. It is essential to intubate using a large-bore endotracheal tube (size 8 mm or larger) whenever feasible. This is performed in preparation for bronchoscopic procedures; however, intubation should not be delayed if a size 8 endotracheal tube is unavailable. Other conservative yet life-saving measures in patients with known lung pathology include patient positioning. Placing the patient in lateral decubitus position with the bleeding lung down is vital to prevent aspiration of blood into the unaffected lung. With bronchoscopic guidance, selective mainstem intubation of the unaffected lung can be utilized to isolate the bleeding lung or a double lumen endotracheal tube can be inserted. Although double lumen endotracheal tubes have been advised, their role in the acute setting is questionable, primarily due to the difficulty of insertion and poor suction capabilities given the small size of the lumen[6].
Following intubation, bronchoscopy should be promptly conducted to identify the cause of hemorrhage and suction aspirated blood, therefore enhancing ventilation-perfusion (V/Q) matching. An endobronchial blocker balloon can be concurrently positioned to isolate the hemorrhaging section and regularly deflated to evaluate hemostasis and the potential recurrence of bleeding. It is essential to document the balloon's depth and regularly observe ventilator waveforms to evaluate potential balloon movement or displacement.
The decision to pursue computed tomography angiography (CTA) before or after bronchoscopy depends on the clinical context and patient stability. Computed tomography (CT) is highly sensitive in localizing the source of bleed, which can be as high as 77%[7,8]. Additionally, the diagnostic yield increases when combined with bronchoscopy. CTA allows for visualization of pulmonary parenchyma and vasculature which can assist in localizing the bleeding vessel.
Both rigid and flexible bronchoscopy can be performed to manage hemoptysis, however rigid bronchoscopy is often not readily available at the bedside. Rigid bronchoscopy can be utilized for better access and passage of large instruments into the trachea and bronchi, suctioning, and lavage. While not readily available, the role of rigid bronchoscopy in patients presenting with life threatening hemoptysis from central airway tumors is lifesaving. Central airway tumors may present with hemoptysis in 20% of cases (Figure 2), and life-threatening hemoptysis is seen in only 3% of cases[9]. Several measures can be undertaken to achieve hemostasis (Table 1). Ice-saline lavage has been routinely used to control bleeding and is believed to cause hemostasis by inducing local vasoconstriction and decreased blood flow to the lavaged segment[3]. Other hemostatic agents that can be instilled are vasopressin analogues such as desmopressin, diluted epinephrine, fibrinogen-thrombin solution and tranexamic acid[10]. Additionally, the use of bronchoscopic tools such as electrocautery, or APC can be utilized to alleviate bleeding malignant or benign lesions. Additionally, other measures such as endobronchial tamponade with a fogarty balloon has been described. Although the above measures can achieve temporary hemostasis, patients with massive hemoptysis should be evaluated for bronchial artery embolization and surgical and interventional radiology consultation should be obtained.
Figure 2 Clinical manifestation.
A: 64 years old man who presented with hemoptysis secondary to adenocarcinoma of the lung with tracheal involvement. Note the tumor occupying the trachea with bleed; B: Rigid bronchoscopy was performed following which a combination of mechanical debulking, argon plasma coagulation and cryo-debulking was performed with resolution of hypoxemic respiratory failure and hemoptysis.
More invasive; requires general anesthesia and operating room
Airway control
Limited
Excellent
Reach
Greater; can access smaller, more peripheral airways
Limited; may not reach distal airways as effectively
Working channel
Narrower
Wider
Suctioning capacity
Limited
Greater
Instrument size
Limited
Larger instruments can be used
Visualization
May be limited in larger airways
Better visualization due to larger instruments
Tamponade
Possible, but less effective
Easier to achieve direct compression
Versatility
Allows for biopsies, lavages, and some therapeutic interventions
Primarily used for airway control and managing massive hemoptysis
Sedation
Often done under conscious sedation
Requires general anesthesia
Recovery time
Faster
Longer due to general anesthesia
Complications
Lower risk
Higher risk, although rare
Patient tolerance
Generally, more comfortable
Less comfortable due to larger scope
ENDOBRONCHIAL ULTRASONOGRAPHY IN THE ICU
Endobronchial ultrasound (EBUS) has emerged as a valuable tool in the diagnosis and management of various pulmonary conditions. It can be used in the assessment of intrathoracic and airway pathology, as well as diagnosis and staging of pulmonary malignancy. The utilized probes are the radial probe and the convex probe. Radial probe EBUS is employed to identify peripheral lung lesions alongside navigational or robotic bronchoscopy to enhance biopsy yield and reduce complication rates[11,12]. Convex probe EBUS on the other hand is more commonly used, especially in sampling mediastinal, hilar, paratracheal, and parabronchial tissue for staging of pulmonary malignancy. Although EBUS was initially utilized in the outpatient setting, its application has expanded to encompass critically ill patients admitted in the ICU.
EBUS involves the insertion of a flexible bronchoscope equipped with an ultrasound transducer. The ultrasound transducer is fitted with a balloon that is connected to a guide sheath, which can be inflated with saline, to serve as an ultrasound wave transmitter and improve visualization. Needle aspiration of mediastinal or pulmonary structures is done under direct ultrasound visualization using a particular needle, sizes of which range between 19G to 22G[13].
In comparison to the outpatient setting, the indications of EBUS in the critically ill are similar. Patients with mediastinal lymphadenopathy who are critically ill may undergo EBUS to evaluate whether an infectious, inflammatory, or neoplastic process is ongoing. In the setting of infectious processes, EBUS guided transbronchial needle aspiration (TBNA) may aid in accurate diagnosis and facilitating timely initiation of appropriate antibiotics and treatment. If there is a concern for malignancy, EBUS can help establish the diagnosis while simultaneously perform tumor staging. The same applies to sampling lung lesions that are proximal and accessible by EBUS.
EBUS and mediastinal lymph node sampling in the ICU
The data on use of EBUS in critically ill patients is scarce and only limited to single center experiences. The largest of these studies was published by Decavèle et al[14], which included 9 critically ill patients, 4 of which were mechanically ventilated. Rapid onsite evaluation of the cytological specimens lead to a change in management of 4 of 6 patients. Koh et al[15] published a case series of 6 patients, all of which were mechanically ventilated. A diagnosis was made in 5 out of the 6 patients, all of which were diagnosed with malignancy, and no major complications were documented. Okachi et al[16] describes a case of pulmonary Cryptococcus in a patient with negative serologies diagnosed by EBUS-TBNA, and prompt initiation of antifungal therapy. Additionally, endoscopic ultrasonography (EUS) is employed to get samples from lymph node stations 5, 6, 8, and 9, which are inaccessible via EBUS. This can be accomplished with a convex probe EBUS scope or an EUS scope. The transesophageal approach may be preferred in patients with tenuous respiratory status who may not tolerate obstruction of their endotracheal tube[17,18]. However, performing EUS requires additional expertise, and is not routinely performed by all interventional pulmonologists.
EBUS and mediastinal vasculature
Mediastinal and hilar vasculature can be visualized with the use of convex probe EBUS, and there is data to suggest that central pulmonary emboli can be diagnosed with EBUS. A pilot study published in 2009 with 32 patients who were diagnosed with PE with CTA, collectively having 101 PE, EBUS was able to detect 96%, and all patients were diagnosed with at least 1 PE. None of the patients developed complications, and the mean procedure time was less than 5 minutes. Of note, the endoscopists were able to access and analyze the CTA prior to the procedure, and none of the patients were on mechanical ventilation[19]. Not all patients may be candidates to undergo pulmonary CTA, or lung perfusion scintigraphy, due to critical illness or contrast allergies, and EBUS may be utilized to diagnose PE at bedside. However more robust data is needed to evaluate the use of EBUS for diagnosing PE, especially in the critical care setting[20].
There are several challenges to the use of EBUS in the ICU. EBUS probes may not be readily available, and EBUS-TBNA requires a multidisciplinary team including respiratory therapists, technologists, cytotechnologists, and an assistant who is familiar with handling the EBUS equipment. Furthermore, performing EBUS in a mechanically ventilated patient may considerably reduce the cross-sectional area of the endotracheal tube, leading to diminished tidal volume, ventilation, alveolar recruitment, and an elevated risk of cardiac compromise. However, this can be mitigated by minimizing suctioning, and avoiding prolonged procedure time, and increasing fractional inspired oxygen (FiO2)[21].
Although data is limited to single centers regarding using EBUS in the ICU, the utility of EBUS is promising, especially in the diagnosis of benign and malignant lesions, in addition to inflammatory and infectious processes. However, its utility should be reserved to specific patients to limit complications and promote effective use of resources.
FOREIGN BODY ASPIRATION
Foreign body aspiration (FBA) is an uncommon but significant cause of hospitalizations, respiratory compromise and ICU admission. Its prevalence is higher in children, and current data suggests that the incidence of non-fatal choking in children under the age of 14 occurs at a rate of 20.4 per 100000. 55.2% of these episodes occur in children < 4 years of age. Data from the National Safety Council demonstrated that approximately 80 percent of patients with FBA were younger than the age of 15. Mortality peaks in children < 1 year of age and adults > 75 years of age[22]. The prevalence of FBA in adults is unknown, and data is limited to single center case series.
Aspirated material can be subdivided into organic and inorganic material. Inorganic FBA includes dental debris, appliances, or prostheses during dental procedures, nails or pins (Figures 2 and 3). Furthermore, iatrogenic aspiration from bronchoscopic tools such as brushes or needles can occur. Organic material (food particles) can be aspirated due to incomplete chewing or poor swallowing. It is important to know the nature of the aspirated foreign body (FB), since organic and inorganic material may require different bronchoscopic tools for removal (Figure 4). Organic foreign bodies constitute bones (i.e., from fish), meat, fruit, and seeds (Figure 5). Extraction of organic foreign bodies tends to be more challenging, since they tend to cause more local inflammation and granulation tissue formation. Additionally, they can expand from airway moisture and worsen obstruction. In contrast, inorganic foreign bodies may cause inflammation, though to a lesser extent, but may cause direct airway injury if sharp or abrasive. Pills, such as iron tablets and potassium chloride pills, when aspirated, can result in significant airway edema and ulceration, as reported in some case reports[23,24].
Figure 5 Bronchoscopy showing aspirated hot dog in the right main stem bronchus which was removed with forceps.
Diagnosis
Clinical presentation varies and depends on the degree of obstruction, location of the FB, and chronicity. The most common symptom is cough, and patients may also present with hemoptysis, foul-smelling sputum, or chest pain[25]. Dyspnea is uncommon and asphyxiation is rare[26]. Patients may have a chronic cough due to distal obstruction and recurrent post-obstructive pneumonia. Other signs suggesting chronicity include unilateral wheeze, and complications from retained foreign bodies such as bronchial stenosis, bronchiectasis, abscess, pneumothorax and pneumomediastinum[25]. Some patients may not recall a history of choking or aspirating[25,26].
If the patient is stable and there is no concern for respiratory compromise, imaging should be obtained. However, if there is suspected asphyxiation, imaging should not delay intervention. A postero-anterior and lateral X-ray of the chest is an appropriate initial test. Of note, most foreign bodies are radiolucent and may not be easily visualized on plain film. However, inorganic foreign bodies, especially metallic objects, are radiopaque and can be visualized[27]. Other signs that may suggest aspiration on imaging are focal hyper-lucency, which may suggest air trapping. Additionally, airspace disease such as consolidation, atelectasis, or mediastinal shift may point towards the presence of foreign bodies. CT could be considered especially if there is a high index of suspicion and chest radiographs are negative. If acutely aspirated, foreign bodies may be more easily visualized in the airway. Although not routinely performed, three-dimensional imaging on a multi-detector multi-slice CT (i.e., virtual bronchoscopy) can be utilized to enhance the detection of aspirated foreign bodies[28].
Management
In cases of life-threatening asphyxiation, initial measures should focus on securing the airway with an endotracheal tube, and if ventilation is unsuccessful, emergent tracheotomy or cricothyrotomy should be considered. Following securement of the airway, laryngoscopic evaluation of the oropharynx is necessary, especially if the FB is in the supraglottic/glottic regions, since one-third of life-threatening asphyxiation occurs due to a supraglottic FB. If supraglottic and visualized, it can be retrieved with Magill forceps[29].
In some cases of life-threatening FBA, and in cases of non-life-threatening FBA, flexible bronchoscopy is the diagnostic and therapeutic procedure of choice. In a retrospective study of 103 patients with FBA, data suggested that rigid bronchoscopy may be more effective in patients with a history of previous failed attempt of retrieving the FB, and in patients with a delayed diagnosis, and especially if the patient has no significant comorbidities[30]. Depending on the FB, proper planning and selection of instruments is prudent. Commonly used instruments are forceps, grasping claws, snares, fish net baskets, magnet-tipped probes, and cryoprobes. Forceps are commonly used for FB extraction and are preferable for less friable foreign bodies such as bones, plastic and metallic objects. The use of forceps in organic material is not recommended, since it can increase the risk of fragmentation and distal displacement of the FB into the airway.
Baskets and snares are used for friable foreign bodies and organic foreign bodies. There are several different types of baskets including fishnet basket, zero-tip retrieval basket, grasping basket and mini-grasping basket. As the basket is contained within its sheath, the sheath is advanced through the working channel, into the airway, between the FB and the airway wall, and beyond the FB. Once the sheath is distal to the FB, the basket is deployed behind the FB, and the basket is pulled back in a rotational axis to snare the FB. The whole apparatus, including the basket, sheath, and bronchoscope are then withdrawn. Fishnet baskets have a similar mechanism.
Cryoprobe is commonly utilized by interventional pulmonologists to biopsy and debulk endobronchial tumors, and in obtaining biopsies of lung parenchyma. Organic FB with moisture can freeze and adhere to the cryoprobe. The cryoprobe is inserted through the working channel, and advanced into the airway until it's in contact with the foreign object. The probe is activated, and the cryogen is released, freezing the FB which adheres to the probe, and can be withdrawn. Also, saline can be instilled onto foreign bodies to enhance freezing and adherence, and this can be applied to inorganic FBs[31].
If large foreign bodies are present within the central airway, or if the patient is at high risk of respiratory compromise, rigid bronchoscopy should be considered, especially if prior attempts with flexible bronchoscopy have failed. Rigid bronchoscopy allows greater access to the central airways and allows gas exchange while simultaneously advancing multiple instruments into the airways including grasping forceps, suction catheters, and even the flexible bronchoscope. Optical forceps could also be used to allow for direct visualization, rigid telescope and rigid forceps can be used for FB retrieval (Table 2).
Advanced through the working channel of the bronchoscope, external grip-handle can be used to open and close the forceps
Common, available, and easy to use. Able to grip thin, small, or flat shaped objects
Risk of fragmentation and distal displacement with organic FB
Snares
Organic and inorganic
Looping or lassoing technique, passed through the bronchoscope to encircle the FB under direct visualization
Useful for larger or irregularly shaped objects such as dental prosthesis, allows for secure capture
Not as readily available. Difficult to use on small or slippery FB
Baskets
Organic and inorganic
Expands to ensnare and retrieve the FB. After its deployed out of the sheath and past the foreign body, the basket is pulled back in a rotation axis to snare the foreign body
Good for retrieving multiple small objects, or irregularly shaped FB
Limited to soft or pliable FB, less effective for large or rigid FB. Friable objects may also fragment and fall out of the basket, in which case a fishnet basket may be more useful
Cryo-probe
Organic, or FB with high moisture/water content
Freezes the FB to the probe, allowing for extraction. The probe along with the bronchoscope is then retrieved through the endotracheal tube
Excellent for organic material, non-fragmenting. Useful for extraction of granulation tissue formed around the FB. Tracheal and bronchial cartilaginous tissue are resistant to cryotherapy
Requires precision, risk of damaging nearby tissue. Care must be taken so that the adjoining mucosa does not form part of the crystal
Following the removal of any FB, the bronchial tree should be reexamined for residual fragments and other foreign bodies. It is important to note that some foreign bodies are too large to be withdrawn through the endotracheal tube, and at times, the bronchoscope, FB, and endotracheal tube must be withdrawn altogether, and the patient may need to be re-intubated.
CAO
CAO is a potentially life-threatening condition which constitutes obstruction of airflow in the trachea and/or mainstem bronchus. This may occur secondary to primary lung malignancy, metastatic disease, or benign disease. Although the incidence of CAO is not well-defined in the literature, more recent data suggests that airway obstruction can be seen in up to 13% of patients with lung cancer, and a further 5% of patients developing CAO upon follow up[32]. Additionally, the incidence of benign conditions that result in CAO such as tracheomalacia (TM) and tracheal strictures is unknown. Multiple classification systems have been implemented in CAO, such as malignant and nonmalignant, intrinsic or extrinsic (i.e., intraluminal or extra-luminal), and dynamic or fixed (such as tracheobronchomalacia or tracheal stenosis, respectively)[33].
Primary lung cancer is the most common cause of CAO. Squamous cell carcinoma more commonly affects the airways; however, adenocarcinoma has also been reported to cause CAO. This occurs due to extension of parenchymal tumor into the airway lumen, or from extrinsic compression of the airway. Primary airway tumors such as carcinoid, adenoid cystic carcinoma, are less common. Other malignant causes are thyroid cancer and esophageal cancer. Benign etiologies are tracheal strictures which may occur secondary to endotracheal tubes or tracheostomy tubes, FBA, and tracheobronchomalacia[33].
Diagnosis
Several radiological clues may point towards CAO, but if life-threatening obstruction is suspected, securing the airway with intubation followed by direct inspection should not be delayed. Clues on the chest radiograph may include tracheal deviation or mediastinal shift from mass effect, tracheobronchial filling defect, or signs of obstruction such as pneumonia, atelectasis, or lobar collapse. A CT scan may show similar findings and may also reveal intraluminal defects in the airways with better characterization of mediastinal and hilar structures. Although pulmonary function test is recommended and may demonstrate characteristic patterns on flow volume loops, it may not be feasible to perform in critically ill patients (Figure 6).
Figure 6 Spirometry showing flattened inspiratory and expiratory loops consistent with fixed upper airway obstruction in a patient with subglottic stenosis.
Management
In patients with non-life-threatening CAO, heliox, which is less dense than inhaled nitrogen and oxygen, may be considered to promote more laminar flow of air through the large airways and at branch points. Heliox can be administered through non-rebreather or non-invasive ventilation. In patients with life-threatening CAO, initial management should be centered on securing the airway with endotracheal intubation and mechanical ventilation. For those where intubation is not feasible or unsuccessful, rigid bronchoscopic intubation should be considered, in addition to emergency cricothyrotomy or tracheostomy if the lesions are at or above the vocal cords. Fiberoptic intubation should also be considered to directly visualize the obstruction and avoid trauma. Intubation with a minimum size 8 mm endotracheal tube is recommended. In severe cases, consideration for veno-venous extracorporeal membrane oxygenation (ECMO) (or venoarterial-ECMO in patients with cardiac dysfunction) can be considered in select patients as a temporizing measure until the CAO can be treated[34]. Management will be further discussed based on whether the CAO is secondary to malignant or non-malignant etiologies.
Non-malignant CAO
There are several causes of non-malignant CAO, the most common being tracheal strictures, which can be a complication of endotracheal or tracheostomy tubes. Non-malignant etiologies can also include FBA, and hyperdynamic collapse from tracheobronchomalacia. Granulation tissue formation from stents, surgical anastomosis (i.e., lung transplant recipients), autoimmune disease such as granulomatosis with polyangitis (Figure 7) or relapsing polychondritis can also lead to CAO. Management of non-malignant CAO is treated differently depending on the underlying disorder.
Figure 7 Computed tomography scans and bronchoscopy.
A: Computed tomography scans showing right upper lobe atelectasis in a 53-year-old patient with granulomatosis with polyangitis; B: Bronchoscopy showing subglottic stenosis in the same patient following which balloon dilatation was performed to relieve the stenosis.
In the setting of subglottic/tracheal stenosis, restoring airway patency can be achieved with either rigid or flexible bronchoscopy. After accessing the airway, radial cuts are made into scar tissue with an electrocautery needle knife, followed by balloon dilatation (Figure 7B). Balloon dilatation alone may be ineffective in some cases, and combining dilation with electrocautery cuts helps avoid use of excessive pressure and iatrogenic mucosal tears with balloon dilation. In patients with more complex stenosis, a circular resection can also be performed followed by dilatation. Following dilation, stents can be deployed to maintain airway patency for benign strictures[35].
TM is characterized by weakness in the wall of the airway, which results in significant airway narrowing during expiration. Several classification systems have been proposed, such as the appearance of the trachea (i.e., crescent, lateral, or circumferential TM), distribution of narrowing (tracheal, bronchial, segmental or diffuse), or etiology (i.e., congenital or acquired)[36].
Published data supports the use of stent placement (Figure 8) in benign CAO, in addition to TM[37]. The choice of stent depends on the clinical scenario. Uncovered self-expanding metallic stents can be used in the short term, are more easily placed, deployed with flexible bronchoscopy, and preserve mucociliary function. However, they have a black box warning for treatment of benign airway disease and are not recommended for long-term use. Additionally, they are not useful for patients with diffuse disease. Silicone stents are firm, durable, and may be easier to reposition. They are preferred for long term use in patients with dynamic airway collapse who are not surgical candidates. However, they do have a higher rate of migration, infection, and impair mucociliary clearance. Furthermore, deployment and removal require rigid bronchoscopy.
Figure 8 Tracheal surgery.
A: Computed tomography scans in an 18-year-old patient showing tracheal rupture following motor vehicle accident; B: With extracorporeal membrane oxygenation support, rigid bronchoscopy was performed followed by placement of Y stent; C: Tracheal tear healed following which Y stent was removed.
APC refers to noncontact electrocoagulation and has been utilized as a more common alternative to contact electrocautery. When a 5000V spark is created at the tip of a probe, a tungsten electrode ionizes argon gas, releasing argon plasma. The argon plasma finds the nearest tissue and results in coagulative necrosis[38]. It has been used in open surgery for treatment of superficial hemorrhage, in addition to gastro-intestinal endoscopy to achieve hemostasis in gastrointestinal bleeds. There are case reports that describe the use of APC to treat airway obstruction resulting from granulation tissue at the site of surgical anastomosis, including airway stents and endoprosthesis, however, it does not result in tumor vaporization and is not ideal for the debulking large masses[38,39].
Malignant CAO
Multiple modalities can be utilized to manage malignant CAO. Management is centered on restoring airway patency by tumor debulking, airway dilation, and preserving patency with stenting in the setting of intraluminal or extraluminal obstruction (Figure 9).
Figure 9 Bronchoscopy showing tumor involvement with squamous cell carcinoma of the lung, which was debulked with electrocautery snaring, and hemostasis was achieved with APC.
Note that tracheal tumor is now debulked and right airway is better visualized (right row). APC: Argon plasma coagulation.
Rigid bronchoscopy is commonly utilized where the airway can be dilated with the barrel of the rigid bronchoscope, and serial dilation can be performed in less urgent cases with either balloons or semi-rigid dilators, which is the preferred method due to less mucosal trauma and consequent granulation tissue formation. Of note, rigid bronchoscopy may be the modality of choice in central tumors where coring out may be the only option, especially if patients are hypoxemic.
Electrocautery has been reported in the management of malignant CAO. In pedunculated masses causing CAO, electrocautery with a snare device can be used to cauterize the stalk and remove the mass. Laser therapy is the mainstay of tumor debulking. A variety of lasers have been utilized in the past, such as the CO2 laser, argon laser, and the Nd:YAG laser. Due to its effective tissue penetration, and minimal absorption by hemoglobin, the Nd:YAG laser is most commonly used[40]. Its use in benign and malignant CAO, and its effectiveness in restoring airway diameter, in addition to symptomatic improvement in patients has been well-documented[40]. APC does not result in tumor vaporization and is not recommended for debulking endobronchial masses[38,39]. It is important to note that all thermal modalities such as laser, electrocautery, or APC require a reduction in FiO2, and not all patients may tolerate such a reduction, limiting their role in such settings. Cryotherapy, on the other hand, may be utilized in this setting (Table 3).
Electrical current applied via a probe to burn or coagulate tissue, electrocautery knives can also be used for tissue resection prior to dilation
Removal of tumors, hemostasis, tissue resection in subglottic stenosis
Precise control, minimal bleeding, and immediate effect. Useful in removal of pedunculated masses (electrocautery snare)
Risk of thermal injury to surrounding tissue, requires low fractional inspired oxygen
Balloon dilation
Balloon catheter inserted and inflated to dilate stenosed airways
Tracheal/bronchial stenosis
Minimally invasive. Can be utilized prior to stent placed to achieve long-term airway patency
Risk of tearing or perforation of the airway
Laser therapy
Used to cut or vaporize obstructive tissue in the airway (Nd:YAG laser most commonly used)
Obstruction from tumors or benign growths
High precision, effective in debulking obstructive lesions
Risk of thermal injury. Risk of damaging surrounding tissue. Costly, not widely accessible
Cryo-probe
Freezing tissue with liquid nitrogen or other cryogenic substance, allowing tissue adhesion and destruction
Treatment and debulking of benign or malignant tumors. Foreign body removal
Minimizes bleeding. Effective for organic tissue
Multiple treatments may be required to debulk large tumors
Argon plasma coagulation
Non-contact thermal coagulation using ionized argon gas
Useful in control of bleeding, useful in granulation tissue formed at the site of surgical anastomosis
Effective for superficial bleeding lesions, less risk of perforation
Does not result in tumor vaporization, and not ideal for debulking large masses
Cryotherapy can be effective in treating malignant CAO. One study showed its utility in resolving hemoptysis in malignant disease in up to 93% of patients, in addition to complete endobronchial tumor removal in 82% of patients[41]. Airway stenting has been used to treat malignant CAO, and stents consist of two types, metallic stents, and silicone stents. Metal stents can be covered or uncovered. For malignant airway obstruction, covered metallic stents are used to prevent tumor ingrowth. Uncovered metallic stents are rarely used and are difficult to extract. As mentioned, silicone stents may require rigid bronchoscopy for placement, have a higher risk of migration, but are more easily removed (Table 4).
Malignant tracheobronchial obstruction. Prevention of tumor ingrowth. Tracheoesophageal fistulas
Limited uses due to significant potential complications. Anastomotic dehiscence following lung transplantation. Can be used for benign conditions, but only short term, however not first line
Prevents tumor ingrowth. Reduces risk of fistula formation. Can be placed with flexible bronchoscopy
Lower risk of migration than covered stents. Can be placed with flexible bronchoscopy. Preserve muco-ciliary function
Easily removable. Less granulation tissue formation compared to metallic stents. Can be used in benign disease. Can be customized during the procedure (i.e., cut to adjust length). Varying shapes, such as cylindrical, or Y-shaped
Disadvantages
Higher migration risk. May obstruct smaller airways or bronchi
Tumor or granulation tissue can grow through the stent, leading to restenosis. Black box warning in benign disease, due to tissue hyperplasia, embodiment in tissue, and consequent occlusion. Difficult to remove
Higher migration risk compared to metallic stents. Requires rigid bronchoscopy for placement
Depending on underlying lung reserve and patient effort, the physiologic effects of CAO occur when at least 50% of airway is occluded[42]. Therapeutic bronchoscopy can be considered successful when at least 50% of airway patency is restored. In ICU patients, the evidence supports the use of modalities mentioned above in patients with CAO and acute hypoxic respiratory failure requiring mechanical ventilation, and favorable outcomes including early extubation and discharge[37,43-46]. The AQuIRE registry highlights the benefit and utility of therapeutic bronchoscopy in malignant CAO, and reports clinically significant improvement in health-related quality of life in up to 42% of patients, and improvement in dyspnea[44].
MANAGEMENT OF PLEURAL DISORDERS IN THE ICU
Pleural effusions
Pleural effusions are common among critically ill patients and may affect up to 50% of patients in the ICU[47]. Depending on the volume of pleural fluid and other factors, patients may complain of dyspnea, chest pain, and cough. The clinical impact of these effusions is not often clear, and the treating clinician must decide if the potential benefits of draining the pleural effusion outweigh the procedural risks[48].
There are numerous causes of pleural effusions which can be divided into either transudative or exudative based on lights criteria or the three-test rule[49,50]. Pleural effusions can be caused by several conditions including heart failure, infections, liver failure, critical illness, mechanical ventilation, pneumonia, malignancy, bleeding/hemothorax, hypoalbuminemia, and volume overload. The patient’s history and physical exam findings along with radiological and laboratory data can all guide clinicians towards the most likely etiology.
Despite the ubiquity of pleural effusions in critically ill patients, there is a lack of prospective trials regarding the safety and efficacy of draining them in the ICU. It is unclear if drainage influences hospital or ICU length of stay or duration of mechanical ventilation[48]. Some studies have demonstrated improvement in oxygenation especially following larger volume thoracentesis (> 500 mL) and low rate of procedural complications[48]. Drainage of pleural effusions is often done for diagnosis and to improve respiratory mechanics, especially in patients who are difficult to wean from the ventilator[51].
Complicated parapneumonic effusion and empyema
Around 20%-40% of patients with pneumonia may develop a parapneumonic pleural effusion and around 5%-10% may progress to empyema[52]. Patients who are at higher risk for pneumonia are also at higher risk for empyema with risk factors including malnutrition, alcohol and drug use, and poor dentition[52]. Bacteria such as streptococcus pneumonia, staphylococcus and oral anaerobes are among the most common culprits of parapneumonic effusions and empyemas[53].
Empyemas associated with pneumonia typically develop in three stages; the first involves an exudative, free flowing fluid that develops due to increased interstitial edema, stage two involves bacterial translocation into the pleural space causing fibrin deposition and loculations, the third and final stage involves organization of the pleural space that may cause a trapped lung and be a nidus for further infections[54]. Other causes constitute trauma, thoracic surgery, esophageal rupture, descending cervical infections may allow bacteria to directly invade the pleural space and cause empyema[53].
Diagnosis
Diagnosis of pleural effusion is often based on physical exam and radiological investigations. Chest X-rays are commonly done in the ICU but may miss small or moderate effusions in approximately half of the patients[54]. Erect chest X-rays are often not feasible in this patient population. CT scans may diagnose incidental effusions and point-of-care ultrasonography is an excellent modality of choice for diagnosis and in guiding clinicians towards possible etiologies of the effusion (Figure 10A)[55].
Figure 10 Computed tomography chest in axial view.
A: Computed tomography (CT) chest in axial view showing presence of hydropneumothorax needing the placement of a 14F chest tube; B: CT chest in axial view of a 45-year-old patient showing pneumothorax with chest tube in left side (arrow); C: With a persistent air leak, endobronchial valves were placed in the lingula as seen on axial and coronal views (arrow).
In patients with suspected infected pleural space, initial diagnosis is typically made by performing a thoracentesis. On ultrasound, a loculated effusion along with thickened parietal pleura, homogenous echogenicity and separation of visceral and parietal pleural are some signs that may suggest empyema[56].
The appearance of frank blood during thoracentesis may indicate the presence of a hemothorax especially in patients who have had recent surgery, trauma, or procedures such as thoracentesis. On ultrasound, findings such as increased echogenicity of pleural fluid and the hematocrit sign, which is the appearance of layering and increasing echogenicity with depth points towards the possibility of a hemothorax[55].
Management
For newly diagnosed pleural effusions, thoracentesis is often performed to visualize and analyze the pleural fluid which helps narrow possible etiologies. However, not every pleural effusion requires thoracentesis. For example, if the underlying etiology is secondary to known disease such as decompensated heart failure, thoracentesis can be held until diuresis has been attempted and has failed to resolve the effusion.
Complicated parapneumonic effusions (CPPE) and empyemas require appropriate antibiotics and drainage of the pleural space. Evacuation of the pleural space is important to allow lung expansion and prevent long-term consequences such as trapped lung. Tube thoracostomy should be performed in CPPE to allow complete and continuous drainage but that may not be possible if there are extensive loculations. Professional society guidelines do not recommend routine use of combination tissue plasminogen activator (TPA) and DNase in patients with complicated pleural effusions or early empyemas[57,58]. British Thoracic Society (BTS) guidelines recommend that it may be used when initial chest tube drainage stops, and a residual pleural collection remains[57].
Procedural considerations
Image guidance with ultrasonography is recommended for thoracentesis or chest tube placement, and the procedure should be done with aseptic technique. It improves success rates, decreases potential complications and is recommended by professional societies[57,58]. This is especially important for patients on mechanical support where inadvertent lung parenchymal puncture may result in a clinically significant pneumothorax. Small bore tubes (< 14 French) have gained favor in recent years for drainage of CPPE or empyema based on evidence that they are similar in efficacy to large bore chest tubes[58]. Once the chest tube is placed, routine flushing is recommended to prevent occlusion and if there is suspicion of inadequate drainage, with evidence of persistent effusion on imaging, TPA-DNase is recommended[59].
PNEUMOTHORAX AND PERSISTENT AIR LEAK MANAGEMENT IN THE ICU
Pneumothorax refers to the presence of air within the chest cavity. It occurs secondary to trauma or may be spontaneous. The latter is further divided into either primary (not associated with any known lung disease) or secondary spontaneous pneumothorax (SSP) (associated with underlying lung disease such as emphysema). Primary spontaneous pneumothorax (PSP) is much more common in younger males compared to females whereas SSP is more likely to occur in older individuals due to increased prevalence of underlying lung disease[60].
Persistent air leak (PAL) is defined as continued air flow from the endobronchial tree into the pleural cavity, exceeding 5-7 days. The exact incidence of PAL is unknown, and the optimal management strategy is unclear. Often, critically ill patients cannot safely undergo complex surgeries therefore minimally invasive therapies to manage PAL have become more prevalent in recent years.
Diagnosis
Patients can present with non-specific symptoms such as dyspnea and chest pain. Diagnosis is made with imaging of the chest. Stable patients can undergo either chest X-ray or CT scans depending on the clinical scenario. For unstable patients, initial bedside ultrasonography is a sensitive test that can alert clinicians towards the possibility of pneumothorax. A hydropneumothorax implies the presence of both air and fluid in the pleural space and may appear as an air-fluid level on chest imaging.
Management
PSP and SSP are managed differently. BTS guidelines recommend a conservative strategy for asymptomatic PSP regardless of size. However, if conservative therapy is not an option, needle aspiration or chest tube insertion can be considered for PSP. For SSP, chemical pleurodesis can be done even after the first episode due to the high rate of recurrence seen in this demographic.
If patients with pneumothorax develop a PAL, professional society guidelines recommend surgical evaluation however chemical or blood patch pleurodesis may be considered in cases where surgery is not an option[57]. The use of endobronchial valves (EBV) to stop PALs (Figure 10B and C) is a more recent development in this field. EBVs are one-way valves which allow airflow out of the bronchus while limiting the inflow of air, which helps resolve PAL. Once the EBVs are in place and effective, cessation of air leak is expected, and the chest tube can be removed. This allows the pleura to heal, and the EBVs can be removed after approximately 6 weeks.
There is a lack of guidelines on the use of EBV for PAL, however several case series have described great success with their use[61]. BTS guidelines recommend thoracic surgery involvement after 48 hours of air leak and recommend surgery as first line. If surgery is not an option, autologous blood patch pleurodesis or EBV can be considered[57]. However autologous blood patch pleurodesis may be associated with empyema, with one study reporting it as a complication in up to 9% of cases[62].
Procedural considerations
Needle aspiration may be attempted in patients with PSP to decrease hospitalizations and is as effective as large bore chest tubes. If needle aspiration fails, small bore chest tubes should be inserted. Although needle aspiration may be attempted in patients with small SSP, it is more likely to fail. If a chest tube is inserted, it may be attached to a Heimlich valve or chest drain, but routine suction is not needed. Suction may be used for patients with PAL or inadequate lung expansion after insertion of chest tube[57].
For PAL, chemical or blood patch pleurodesis may be attempted when surgery is not an option. In the United States, a humanitarian device exemption from the Federal Drug Administration (FDA) exists for the use of EBV in the management of PAL. Currently only the Spiration valve is approved for this indication whereas the Zephyr valve is still under the process of approval for use in PAL.
TRACHEOSTOMY
Tracheostomy is a commonly performed procedure in patients who require prolonged mechanical ventilation due to respiratory insufficiency. Tracheostomy can be performed surgically or percutaneously, and percutaneous tracheostomy (PT) has become more prevalent and performed at bedside by interventional pulmonologists and intensivists in the ICU.
Procedural considerations
Common indications for PT are inability to wean patients off the ventilator, or chronic respiratory failure due to neurological or neuromuscular disease. Other indications include trauma, angioedema, malignancy, or patients with obstructive sleep apnea refractory to conventional therapies. With reference to surgical tracheostomy, there are several relative contraindications which include obesity, coagulopathy, inability to extend the neck (i.e., trauma or C-spine surgery), and high ventilator support. In contrast, there is data to suggest that the percutaneous approach can be performed safely in these high-risk patients[63]. Additionally, there is data to suggest that there is no significant difference in mortality, bleeding, false passage, or subglottic stenosis between surgical and PT[64,65]. Furthermore, PT has been shown to have a lower rate of wound infection and stomatitis[65].
Procedural technique
PT is performed by insertion of a tracheal cannula using a modified Seldinger approach through the anterior tracheal wall between the 2nd and 3rd tracheal rings. After the trachea is accessed with a needle, a guidewire is inserted, and dilation is performed until the stoma is large enough for the tracheostomy tube to be introduced. This can be done with simultaneous intraluminal visualization by using a bronchoscope , or with ultrasound guidance[66,67].
Tracheostomy results in patient comfort, improved work of breathing due to less airway resistance, decreased need for sedation, and decreased ICU length of stay, and should always be considered in patients with prolonged dependance on mechanical ventilation.
PERCUTANEOUS GASTROSTOMY TUBE PLACEMENT
Critically ill patients who need prolonged life-sustaining support are in a state of severe catabolism, and establishing enteral access to start nutrition is paramount[68]. Percutaneous endoscopic gastrostomy (PEG) tubes are a safe and effective method to provide enteral nutrition to patients who require prolonged enteral access.
Procedural considerations
Indications for PEG tube placement includes patients that require long-term nutritional support and have a functional gastrointestinal tract, without sufficient oral intake. The most common indication is dysphagia secondary to neurological diseases such as stroke, amyotrophic lateral sclerosis and Guillain-Barré syndrome or dementia. Other indications include upper gastrointestinal obstruction due to malignancy or trauma. Contraindications include coagulopathy, sepsis, severe ascites, peritonitis, peritoneal carcinomatosis, and gastric outlet obstruction[69].
Procedural technique
There are several techniques for gastrostomy tube insertion, and these can be categorized into endoscopic guided (peroral) techniques, and direct percutaneous techniques. The peroral technique utilizes endoscopy to guide gastrostomy tube insertion, in addition to transillumination and insufflation of the stomach to align the gastric wall to the abdominal wall[70]. Of note, it may be difficult in patients with upper gastrointestinal pathology which limits the passage of the endoscope. Percutaneously, gastrostomy tubes can be placed with ultrasound guidance [percutaneous ultrasound gastrostomy (PUG)]. With the use of an existing orogastric or nasogastric tube, the stomach is insufflated, and a specialized orogastric tube with a magnet is advanced to the stomach, the gastric wall can be aligned with the abdominal wall using an external handheld magnet, and the gastrostomy tube is inserted using Seldinger technique[71].
There is no data to compare patient outcomes with each technique. It is important to note that percutaneous ultrasound gastrostomy requires less equipment and is less costly. Additionally, the point of care ultrasound magnet-aligned gastrostomy system that was developed is only FDA approved for patients with a body mass index between 30-35 and abdominal wall thickness less than 4.5 cm. Furthermore, data is lacking to evaluate the safety and efficacy of this technique in comparison to the standard PEG technique[71,72].
Gastrostomy tubes are becoming more frequently placed by interventional pulmonologists following tracheostomy. This is done to minimize risks associated with sedation, and both procedures can be coordinated by the same proceduralist. One prospective study evaluated the use of PEG tube placement with endoscopic guidance performed by interventional pulmonologists and reported a 97.6% success rate[73]. Another retrospective study demonstrated a success rate of 97% when performed by interventional pulmonologists[74].
In summary, PUG tube placement is being increasingly performed by interventional pulmonologists, this can limit costs, and minimize risks associated with sedation if performed following tracheostomy. This translates to lower duration of stay in the ICUs with associated lower hospitalization costs.
CONCLUSION
IP with its rapid advancements is fast becoming an important subspecialty in the management of critically ill patients, particularly in patients with hypoxemic/hypercapnic respiratory failure due to several reasons. While this manuscript outlines several of the roles an interventional pulmonologist can offer in the critical care environment, the list is not all encompassing and with the different technological advancements that are fast upcoming within IP, the advantages and benefits of IP within critical care is likely to increase. Moreover, future studies comparing the bedside techniques performed by IP vs interventional radiology or surgery should be performed to assess cost-effectiveness within the ICU.
Footnotes
Provenance and peer review: Invited article; Externally peer reviewed.
Peer-review model: Single blind
Specialty type: Critical care medicine
Country of origin: United States
Peer-review report’s classification
Scientific Quality: Grade B, Grade D
Novelty: Grade B, Grade B
Creativity or Innovation: Grade B, Grade C
Scientific Significance: Grade B, Grade C
P-Reviewer: Huang DB; Liang GD S-Editor: Luo ML L-Editor: A P-Editor: Zhang YL
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