Innovative Management of Severe Tracheobronchomalacia Using Anterior and Posterior Tracheobronchopexy

Claire Lawlor, MD ; Charles Jason Smithers, MD; Thomas Hamilton, MD; Christopher Baird, MD; Reza Rahbar, DDS, MD; Sukgi Choi, MD* ; Russell Jennings, MD*

Objectives/Hypothesis: Combined anterior and posterior tracheobronchopexy is a novel surgical approach for the management of severe tracheobronchomalacia (TBM). We present our institutional experience with this procedure. Our objective was to determine the utility and safety of anterior and posterior tracheopexy in the treatment of severe TBM. Study Design: Retrospective chart review. Methods: All patients who underwent anterior and posterior tracheopexy from January 2013 to July 2017 were retrospectively reviewed. Charts were reviewed for indications, preoperative work-up, tracheobronchomalacia classification and severity, procedure, associated syndromes, synchronous upper aerodigestive tract lesions, and aberrant thoracic vessels. Main outcomes measured included improvement in respiratory symptoms, successful extubation and/or decannulation, vocal fold immobility, and new tracheotomy placement. Results: Twenty-five patients underwent anterior and posterior tracheopexy at a mean age of 15.8 months (range, 2–209 months; mean, 31 months if 2 outliers of 206 and 209 months included). Mean length of follow-up was 26.8 months (range, 13–52 months). Indications for surgery included apneic events, ventilator dependence, need for positive pressure ventilation, tracheotomy dependence secondary to TBM, recurrent pneumonia, and exercise intolerance. Many patients had other underlying syndromes and synchronous upper aerodigestive tract lesions (8 VACTERL, 2 CHARGE, 1 trisomy 21, 1 Feingold syndrome, 17 esophageal atresia/tracheoesophageal fistula, 20 cardiac/great vessel anomalies, 1 subglottic stenosis, 1 laryngomalacia, 7 laryngeal cleft). At preoperative bronchoscopy, 21 of 25 patients had >90% collapse of at least one segment of their trachea, and the remaining four had 70% to 90% collapse. Following anterior and posterior tracheopexy, one patient developed new bilateral vocal- fold immobility; one patient with a preoperative left cord paralysis had a new right vocal-fold immobility. Postoperatively, most patients had significant improvement in their respiratory symptoms (21 of 25, 84%) at most recent follow-up. Three patients with preexisting tracheotomy were decannulated; two patients still had a tracheotomy at last follow-up. Two patients required new tracheotomy for bilateral vocal-fold immobility. Conclusions: Combined anterior and posterior tracheopexy is a promising new technique for the surgical management of severe TBM. Further experience and longer follow-up are needed to validate this contemporary approach and to minimize the risk of recurrent laryngeal nerve injury. Key Words: tracheomalacia, bronchomalacia, tracheopexy, bronchopexy. Level of Evidence: 4 Laryngoscope, 130:E65–E74, 2020

INTRODUCTION approximately one in 2,500 live births. Tracheal collapse Tracheobronchomalacia (TBM) is a disease state can result from intrinsic weakness of the airway or from characterized by collapse or compression of the trachea extrinsic compression.1,2 Intrinsic weakness is rare and is and mainstem bronchi on exhalation, with an incidence of associated with weak or soft cartilage. More commonly, the cartilage takes an abnormal shape and/or there is dynamic collapse of the posterior wall of the trachea.2 From the Department of Otolaryngology (C.L.), Children’s National Early histopathologic studies of the trachea in children Medical Center, Washington, DC; and the Department of Surgery (C.J.S., with TBM/tracheoesophageal fistula (TEF) postmortem T.H., R.J.), Department of Cardiac Surgery (C.B.), and Department of Otolaryngology and Communication Enhancement (R.R., S.C.), Boston found a decrease in the normal 4.5:1 ratio of cartilage to Children’s Hospital, Boston, Massachusetts, U.S.A. posterior membrane muscle, and historically this has Editor’s Note: This Manuscript was accepted for publication on been used to characterize TBM.1 Excessive dynamic air- February 27, 2019. fi *S.C. and R.J. are co-senior authors. way collapse is a relatively new term speci cally used to Presented at the 2018 ASPO Annual Meeting, National Harbor, describe patients with airway narrowing caused by coap- Maryland, U.S.A., April 20, 2018. fi tation of a wide, mobile posterior membrane into the air- Winner of the Charles Ferguson Award, rst place, for best clinical 3 manuscript at the 2018 ASPO Annual Meeting, National Harbor, Maryland, way lumen. The trachea and bronchi can be extrinsically April 20, 2018. compressed by structures such as normal or aberrant vas- fi fl The authors have no funding, nancial relationships, or con icts of culature, thyroid goiters, congenital tumors and cysts, interest to disclose. 4 Send correspondence to Sukgi S. Choi, MD, Department of Otolar- and the spine or sternum. TBM is commonly associated yngology, Boston Children’s Hospital, 300 Longwood Ave BCH3129, with other syndromes or synchronous airway lesions, Boston, MA 02115. E-mail: [email protected] such as VACTERL, esophageal atresia (EA)/TEF, and – DOI: 10.1002/lary.27938 laryngeal and laryngotracheal cleft.1,2,5 7

Laryngoscope 130: February 2020 Lawlor et al.: Tracheopexy for Severe Tracheobronchomalacia E65 TBM usually presents within the first 2 to 3 months ventilator or oxygen weaning, extubation and/or decannulation, of life.2,8 The most common presentation includes barking vocal-fold immobility, and new tracheotomy placement. cough and biphasic or expiratory stridor. Recurrent or prolonged respiratory infections, feeding difficulties, increased work of breathing, wheezing, cyanosis, and/or apnea may also be present.2,9 TBM can be divided into Decision Making for Treatment of TBM mild, moderate, and severe forms. Mild forms can present An algorithm for the use of anterior and posterior tracheopexy in the treatment of severe TBM is shown in Figure 1. Work-up for as recurrent or prolonged respiratory infections. Mild TBM is based on patient signs and symptoms, including barky TBM may have a self-limited course, which may improve cough, recurrent respiratory infections, prolonged respiratory infec- ’ as the child s airway grows, sometimes by age 2 years, tions, exercise intolerance, development of bronchiectasis, and 10 and therefore may go undiagnosed. Moderate and ALTE/BRUE. severe cases present with expiratory stridor, barky cough, The diagnosis of TBM is made during dynamic, three-phase recurrent and prolonged infections, and apneic apparent bronchoscopy, which is the preferred method of the pediatric sur- life-threatening event (ALTE)/brief resolved unexplained geons at our institution, who participated in or performed the event (BRUE) episodes.11 The mortality of severe TBM bronchoscopies on this cohort.14 The first phase of the dynamic may be as high as 80%.1 Direct bronchoscopy is the gold bronchoscopy is performed using a ventilating bronchoscope with standard for diagnosis of TBM, with multidetector com- the patient taking spontaneous, shallow breaths. This allows for evaluation of static compression of the trachea and bronchi, as puted tomography (MDCT) serving as an adjunct source well as identification of synchronous airway anomalies. In the of information.12 Historically, a dynamic reduction in the tracheal diameter of more than 50% associated with classic symptoms was used as the threshold to diagnosis of TBM on bronchoscopy.2 Primary treatment modalities for severe TBM failing expectant management have included tracheotomy often with positive pressure ventilation (PPV) to “stent” the col- lapsing airway, tracheal stents to hold the airway open, and anterior aortopexy to suspend the vessel and allevi- ate much of the external vascular compression on the anterior trachea.1,13 Great strides have been made within the past 5 to 10 years to advance the surgical management of TBM. Posterior tracheopexy, which tacks the posterior membranous wall of the trachea to the spine, has demonstrated success in correcting posterior membrane intrusion.11,14–16 However, a subset of patients may bene- fit from both anterior aortopexy, anterior tracheopexy, and posterior tracheobronchopexy. We present a cohort of patients requiring this novel surgical combination and review their operative criteria and surgical outcomes.

MATERIALS AND METHODS We retrospectively reviewed all patients who underwent anterior and posterior tracheobronchopexy at Boston Children’s Hospital from January 2013 to July 2017 under an approved institutional review board protocol (IRB-P00026671). All patients who underwent anterior and posterior tracheobronchopexy during this time were included. Anterior and posterior tracheobronchopexy procedures were performed by the Esophageal and Airway Treatment team at Boston Children’s Hospital, which consists of three primary pediatric surgeons, one pediatric car- diothoracic surgeon, one pediatric pulmonologist, two pediatric gastroenterologists, and two pediatric otolaryngologists. All pre- and postoperative dynamic bronchoscopies were performed by the pediatric surgeons and/or pediatric otolaryngologists. A review of patient records was conducted, and data were collected, including patient age at the time of surgery, gender, presenting symptoms, comorbid conditions, synchronous direct laryngotracheobronchoscopy ﬁndings, surgical procedures, time between operations, total number of operations, resolution of preoperative respiratory symptoms, complications of anterior/ Fig. 1. Management algorithm for anterior/posterior tracheopexy. posterior tracheobronchopexy, and length of follow-up. Main out- ALTE = apparent life-threatening event; BRUE = brief resolved comes measured were patient speciﬁc and included improvement unexplained event; CTA = computed tomography angiography; in apnea, frequency of respiratory illnesses, exercise intolerance, TBM = tracheobronchomalacia.

Laryngoscope 130: February 2020 Lawlor et al.: Tracheopexy for Severe Tracheobronchomalacia E66 second phase of bronchoscopy, the aim is to see the patient’s airway during valsalva or cough to assess maximum dynamic motion and collapse during expiration (Fig. 2). This is achieved by lightening the anesthetic until the patient becomes sensitive to stimulation in the airway (either via the bronchoscope itself or a flexible suction catheter) and begins to cough. In the final phase of bronchoscopy, all secretions are removed, and the airway is examined while the patient is sedated with the airway distended to 40 cm H2O (30 cm H2O in neonates). This procedure facilitates evaluation of the posterior membrane for TEF and tracheal diverticulum. Patients who are candidates for surgery based on clinical findings and dynamic, three-phase bronchoscopy then undergo a dynamic airway MDCT angiogram with artery of Adamkiewicz protocol (Fig. 3) to understand the loca- tions of the mediastinal structures, identify vascular or mass compression, and plan surgical intervention. Conservative management is first attempted for all patients diagnosed with TBM. Medical therapies include hypertonic saline nebulizer treatments to thin airway secretions and facilitate clear- ance, inhaled ipratropium bromide to decrease secretions, and chest physiotherapy. Inhaled low-dose corticosteroids and antibiotics to decrease airway inflammation are minimized and used only during

Fig. 3. Dynamic airway computed tomography angiogram with artery of Adamkiewicz (AoA) protocol. The AoA is the primary blood supply to the thoracolumbar spine; the aorta supplies the AOA, which feeds the anterior spinal artery. Oblique coronal 1.3- to 1.5-mm-thick maximum intensity projections are reconstructed from the phase where the AoA is identiﬁed. The AoA is identiﬁed as a classic “hairpin loop” (red asterisk) within the spinal canal as it arises from an intercostal artery and feeds into the anterior spinal artery.

active infections. Continuous positive airway pressure (CPAP) and bilevel positive airway pressure are noninvasive treatments for TBM and can be delivered via face masks, endotracheal tubes, or tracheotomy tubes. However, dependence on PPV and/or tracheotomy, recurrent respiratory infections precipitating multiple hospitalizations, ALTE/BRUE, and, more often in older patients, exercise intolerance that persists despite conservative management will prompt surgical management. The duration of conservative management attempted is dependent on individual presentation and severity of symptoms and is usually 1 month at minimum. Itisimportanttonotethatwealso perform anterior aortopexy in isolation for TBM at our institution; this decision is made based on individual patient presentation and bronchoscopic findings. In patients with significant posterior membrane intrusion without need for cardiac surgery, we first support the posterior membrane using posterior tracheobronchopexy. Typically, the posterior tracheobronchopexy is performed through the right fourth intercostal space (in those patients with a left aortic arch), retracting the lungs anteri- orly and rotating the esophagus laterally. Posterior tracheopexy is performed by passing autologous pledgeted polypropylene sutures into but not through the posterior tracheal membrane and securing them to the anterior longitudinal ligament of the spine. The pledgets are made from pleura, pericardium, or fibrousscartissueasopposed to synthetic material and protect the delicate structures from suture Fig. 2. (A) Severe tracheobronchomalacia with anterior compression fl and posterior intrusion on dynamic bronchoscopy. (B) Airway damage. The sutures are placed under intraoperative exible bron- patency after anterior and posterior tracheopexy on dynamic bronchoscopic visualization, which allows the surgeon to assess the result choscopy during Valsalva or cough. (Photos are from different of each suture on the airway while avoiding suture placement patients.) into the lumen of the trachea. The number and placement of

Laryngoscope 130: February 2020 Lawlor et al.: Tracheopexy for Severe Tracheobronchomalacia E67 TABLE I. Surgical Indications for Anterior and Posterior Tracheopexy, Often Multifactorial.

Surgical Indication N (%)

Recurrent respiratory infections 12 (48) Ventilator/PPV dependence 11 (44) Increased work of breathing/respiratory distress 8 (32) ALTE/BRUE 5 (20) Tracheotomy dependence 5 (20) Exercise intolerance 2 (8)

ALTE = apparent life-threatening event; BRUE = brief resolved unexplained event; PPV = positive pressure ventilation.

with flexible bronchoscopy to assess the effects of the correction. Illustration of thoracic structures before and after anterior and posterior tracheopexy can be seen in Figure 4. In patients who require cardiac surgery on bypass, the cardiac and tracheal surgeries can be combined into one operation guided by the intraoperative bronchoscopy. A sternotomy approach affords excellent exposure for cardiac surgery and anterior aortopexy. The anterior tracheopexy sutures are guided by intraoperative bronchoscopy to optimize the anterior airway support. Unfortunately, access to the posterior trachea via a sternotomy is very difficult. The child may require cardiac bypass with the heart decompressed. The trachea can then be rotated 90 to place the posterior tracheopexy sutures. The sutures cannot eas- ily be placed under bronchoscopic guidance, although suture placement can be verified after the trachea is rotated back to its anatomical position. Mobilizing the esophagus for access to the spine from the anterior approach is challenging and places the vagus and recurrent laryngeal nerves (RLNs) at greater risk of injury than does a thoracoscopic or thoracotomy approach. The rationale for performing the anterior and posterior tracheopexy versus just anterior tracheopexy at the time of cardiac Fig. 4. Illustrations of thoracic structures before (A) and after (B) anterior surgery is related to the complexities associated with exposure. At and posterior tracheopexy. A = aorta; E = esophagus; Sp = spine; St = present, if preoperative dynamic bronchoscopy demonstrates signifi- sternum; T = trachea; Th = Thymus. cant posterior membrane intrusion, we will perform anterior and posterior tracheopexy at the time of cardiac surgery. Occasionally, anterior tracheopexy will be performed at the time of cardiac sutures is guided by the patient’s anatomy; a typical range is six to 24 interrupted sutures. At the end of the procedure, negative fl pressure is applied to the airway with exible bronchoscopy to TABLE II. fi visualize the airway and con rm noncollapsibility. This tech- Syndromes and Anatomical Anomalies Associated With Patients nique significantly improves or resolves symptoms in approxi- Undergoing Anterior and Posterior Tracheopexy. mately 90% of our patients with severe TBM, and they do not require anterior aortopexy/tracheopexy.15 No. In those patients who do not have complete resolution of Syndromes symptoms and continue to have demonstrable TBM on dynamic, three-phase bronchoscopy, an anterior approach is utilized to VACTERL 8 perform anterior tracheopexy. A mini-sternotomy allows approach CHARGE 2 to all the structures in the mediastinum. Initially, the thymus is Trisomy 21 1 removed to improve access in the anterior mediastinum. With Feingold 1 intraoperative flexible bronchoscopy used to guide the surgeon, Synchronous anomalies ascending aortopexy is performed by opening the pericardium and suspending the ascending aorta from the sternum. This may be all Cardiac/great vessel 20 that is needed to improve the airway. The innominate artery may Subglottic stenosis 1 require suspension as well. Often, these maneuvers are not enough Laryngomalacia 1 to adequately open the airway due to cartilage malformation or Laryngeal cleft compression. In those patients, the anterior wall of the trachea is Type 1 2 exposed and direct anterior tracheopexy is performed, supporting the trachea to the sternum. Due to the prior posterior membrane Type 2 4 fixation after the posterior tracheopexy, usually very little move- Type 3 1 ment of the anterior trachea is needed to optimize airway anatomy. Unilateral vocal-fold immobility 3 After sternal closure, the airway is tested under negative pressure

Laryngoscope 130: February 2020 Lawlor et al.: Tracheopexy for Severe Tracheobronchomalacia E68 TABLE III. Patient Characteristics, Comorbidities, Surgical Indications, Procedures, and Outcomes.

Age Surgical Preoperative Residual Operative Postoperative TVC Patient (Mo) Comorbidities Prior Procedures Indications TVC Mobility TBM Classiﬁcation Procedure 1 Symptoms Procedure 2 Interval Other Procedures Outcomes Mobility

1 6 CHARGE, type II EA/TEF repair; Prolonged Mobile 80% collapse of Posterior Persistent CPAP Anterior tracheopexy, 25 Tracheotomy; type II 50%–70% collapse L Immobile bilaterally laryngeal cleft, EA/ repair of intubation, bilaterally midtrachea, tracheopexy, EA/ anterior aortopexy, laryngeal cleft mainstem TEF, tracheal coarctation of extubation to complete TEF repair, and innominate repair bronchus, still on diverticulum, the aorta, PDA BiPAP 19/13, collapse at distal resection of artery pexy CPAP 6, no coarctation of aorta, ligation desaturations/ trachea; L tracheal further aspiration bicuspid aortic bradycardia mainstem diverticulum or desaturations/ valve, VSD, large with agitation bronchus >50% bradycardia with PDA, BPD despite PPV, collapse agitation recurrent pneumonia 2 56 VACTERL, type II EA/TEF repair; Trach Mobile Complete collapse of Posterior Persistent CPAP Anterior tracheopexy, 359 Type II laryngeal cleft <50% collapse in all Mobile bilaterally laryngeal cleft, EA/ tracheotomy dependence, bilaterally mid- and distal tracheopexy, anterior aortopexy segments on TEF, tracheal recurrent trachea; L resection of DLB, diverticulum, respiratory mainstem tracheal decannulated aberrant R infection bronchomalacia diverticulum, subclavian artery >50% repair of aberrant subclavian artery 3 209 Double aortic arch Division of double Dyspnea on Mobile >70% collapse distal Anterior tracheopexy, NA NA N/A N/A Improved exercise Mobile bilaterally aortic arch; exertion/ bilaterally trachea and R posterior intolerance, suspension of exercise mainstem tracheopexy, resolved frequent aortic arch intolerance, bronchus, anterior pneumonias recurrent external aortopexy, R infections compression mainstem bronchopexy

4 5 Double aortic arch, EA/ EA/TEF repair; BiPAP L immobile Midtrachea complete Anterior tracheopexy, NA NA NA Tracheotomy Weaned to CPAP New R TVC immobility, TEF, BPD double aortic settings 14/8 before collapse posterior PEEP 6 immobile bilaterally arch repair tracheopexy, tracheal diverticulum resection, repair of double aortic arch 5 12 VACTERL, EA/TEF None Repeated Mobile Complete collapse at Posterior Recurrent Revision posterior 284 NA No reintubations or Mobile bilaterally intubations for bilaterally midtrachea, tracheopexy, TEF respiratory tracheopexy, respiratory respiratory innominate repair, tracheal infections anterior distress, failure compression diverticulum tracheopexy, recurrent severe/ repair anterior aortopexy prolonged respiratory infections resolved 6 10 VACTERL, EA, None Ventilator Unknown >90% collapse at Posterior Respiratory Anterior aortopexy, 119 NA Doing well, on room Initially bilateral dextrocardia, ASD dependence, proximal/ tracheopexy, EA distress anterior tracheopexy air weakness, improved intubated midtrachea repair, excision of tracheal diverticulum 7 13 Hypoplastic aortic arch, Hypoplastic aortic Trach Mobile Complete collapse of Posterior Profound Anterior tracheopexy 15 NA Persistent severe Mobile bilaterally VSD, severe distal arch/VSD dependence, bilaterally mid/distal tracheopexy desaturations distal bronchomalacia repair; severe trachea, with agitation bronchomalacia, tracheotomy desaturations/ bronchomalacia despite PEEP PEEP still 12, still cyanosis, needs trach PEEP 12

8 16 EA/TEF, ASD, L-sided EA/TEF repair w/ L Apneic episodes/ Mobile >80 collapse distal Anterior tracheopexy, NA NA NA NA No further apneic Mobile bilaterally spit ﬁstula, Feingold, spit ﬁstula ALTEs bilaterally trachea, posterior episodes, doing type I cleft complete tracheopexy, well collapse bilateral anterior mainstem bronchi aortopexy, RPA pexy, resection of TABLE III. (Continued)

tracheal diverticulum, ASD 9 203 EA/TEF, hypoplastic R Tracheotomy, EA/ Trach Mobile Complete collapse in Anterior tracheopexy, NA NA NA NA Decannulated, on Mobile bilaterally lung, hiatal hernia, TEF repair, dependence, bilaterally mid/distal trachea anterior room air, doing dextrocardia, hiatal hernia CPAP aortopexy, well VACTERL repair posterior tracheopexy, resection of tracheal diverticulum, R pneumonectomy 10 40 EA/TEF, VACTERL, EA repair, PDA ALTEs, recurrent Mobile Complete collapse of Anterior tracheopexy, Continued Posterior tracheopexy, 1,138 NA No further severe/ Mobile bilaterally VSD, PDA ligation respiratory bilaterally the distal trachea anterior recurrent resection of tracheal prolonged infections aortopexy, VSD/ respiratory diverticulum respiratory PFO repair infections infections, ALTEs resolved

11 14 EA EA repair Respiratory Mobile Complete collapse of Anterior tracheopexy, Persistent Posterior tracheopexy 70 NA No further severe/ Mobile bilaterally distress, bilaterally distal trachea, anterior difﬁculty prolonged recurrent anterior aortopexy breathing, respiratory respiratory compression recurrent infections, infections infections increased WOB resolved 12 6 EA/TEF, SGS, type II EA/TEF repair, Trach Mobile Complete collapse of Posterior Continued trach Anterior tracheopexy, 174 Type II laryngeal cleft Decannulated, on Mobile bilaterally laryngeal cleft tracheotomy, dependence, bilaterally mid/distal tracheopexy, and CPAP anterior aortopexy repair, LTR room air, no type II recurrent trachea, bilateral resection of dependence further severe/ laryngeal cleft respiratory mainstem bronchi tracheal prolonged repair infection diverticulum respiratory infections 13 9 EA, tracheal None Recurrent Mobile Complete collapse of Posterior Residual Anterior tracheopexy, 134 NA On room air, no Mobile bilaterally diverticulum, pHTN, infections, bilaterally mid/distal tracheopexy, EA respiratory anterior aortopexy further severe/ ASD, VACTERL respiratory trachea, bilateral repair, excision of distress, prolonged distress, need mainstem bronchi tracheal infections respiratory for CPAP diverticulum infections

14 5 EA, tracheal EA repair Ventilator Unknown Complete collapse of Posterior Failed extubation Anterior tracheopexy, 61 NA Extubated to room Mobile bilaterally diverticulum, dependence, midtrachea, L tracheopexy, EA anterior aortopexy air, doing well VACTERL intubated mainstem repair, excision of collapse; severe tracheal anterior diverticulum compression 15 11 R aortic arch, None Recurrent Mobile 80% collapse of Anterior tracheopexy, NA NA NA NA No further severe/ Mobile bilaterally circumﬂex aorta respiratory bilaterally distal trachea, posterior prolonged infections, severe bilateral tracheopexy, respiratory respiratory mainstem bronchi aortopexy, aortic infections, distress collapse arch increased WOB reconstruction resolved

16 3 TOF, aberrant left None CPAP dependent, Unknown Complete collapse at Anterior tracheopexy, NA NA NA NA Off positive pressure Mobile bilaterally subclavian, respiratory carina, mainstem posterior ventilation, on pulmonary valve distress, bilaterally tracheopexy, room air, doing regurgitation and cyanosis aortoplasty, well stenosis with dual closure of VSD LAD of the R aortic arch 17 3 R aortic arch, large None Desaturations, Mobile Complete collapse at Anterior tracheopexy, Persistent CPAP Anterior tracheopexy 64 Supraglottoplasty Off CPAP, doing Mobile VSD, laryngomalacia cyanosis, bilaterally mid/distal trachea posterior well, on room air bilaterally respiratory and L mainstem tracheopexy, distress bronchus aortic arch reconstruction, VSD/ASD closure

18 39 VACTEREL, ASD, type Tracheotomy, Trach Mobile Complete collapse of Posterior Continued anterior Anterior tracheopexy, 15 NA Still has trach, still Mobile bilaterally II laryngeal cleft, ASD repair dependence, bilaterally mid/distal trachea tracheopexy collapse, anterior aortopexy requires anoxic brain injury frequent desaturations intermittent with autonomic desaturations CPAP, ALTEs instability, seizure to 10%, and severe disorder, chronic cyanotic desaturations hypoxemic episodes, resolved respiratory failure ALTEs 19 2 TOF, absent pulmonary None Intubated at birth, Unknown Complete collapse of Anterior tracheopexy, Continued Posterior tracheopexy 72 NA On room air, doing Mobile bilaterally valve severe airway distal trachea, R TOF repair, high-ﬂow O2 well compression mainstem resection of requirements, bronchus branch main PA, airway resection of compression ascending aorta, LeCompte procedure 20 9 EA/TEF, PDA, type III EA/TEF repair x2, ALTE, recurrent L immobile Complete collapse Anterior tracheopexy, NA NA NA NA On room air, no L immobile before, laryngeal cleft, L PDA ligation, respiratory before mid/distal trachea posterior further severe/ R mobile TVC immobility laryngeal cleft infections, tracheopexy, prolonged repair ventilator aortopexy, repair respiratory dependence tracheal infections or diverticulum, ALTEs resection mediastinal cyst 21 16 EA/TEF, type I laryngeal EA repair ALTE, cyanosis Unknown Complete collapse Posterior Recurrent Anterior aortopexy, 67 Type I laryngeal cleft On room air, no Mobile bilaterally cleft, VACTERL with feeding midtrachea tracheopexy, EA/ respiratory anterior tracheopexy repair further severe/ TEF repair, infections prolonged removal of respiratory tracheal FB infections, no further ALTEs 22 20 EA/TEF, PFO, EA/TEF repair Recurrent Mobile Complete collapse Posterior Recurrent Aortopexy, anterior 207 NA On room air, doing Mobile bilaterally bifurcating R respiratory bilaterally mid/distal trachea tracheopexy, respiratory tracheopexy well, no further innominate artery infections, resection of infections infections respiratory tracheal distress diverticulum

23 44 Unbalanced complete L pulmonary artery Recurrent L immobile Complete collapse Posterior NA NA NA NA On room air, no L immobile before, R AV canal defect, EA/ plasty, L AV respiratory before mid/distal tracheopexy, further mobile TEF; trisomy 21 valve plasty, infections trachea, L anterior hospitalizations closure of L AV mainstem tracheopexy, for respiratory canal; bronchus posterior infections Norwood; aortopexy, Glenn; EA/TEF anterior repair aortopexy, resection tracheal diverticulum, aortic coarc patch repair, pulmonary artery reconstruction 24 18 Circumﬂex aortic arch None Recurrent Mobile >80% narrowing Posterior NA NA NA NA No further severe/ Mobile bilaterally respiratory bilaterally distal trachea w/ tracheopexy, prolonged infections, posterior pulsatile anterior respiratory exercise mass tracheopexy, infections intolerance aortic uncrossing

25 6 EA/TEF, ASD/VSD, PV None Respiratory Mobile >80% collapse at Posterior Respiratory Anterior tracheopexy, 140 NA On room air, no Mobile bilaterally stenosis, CHARGE, distress bilaterally distal trachea tracheopexy, EA distress, anterior aortopexy, further intestinal requiring repair Foker 1 recurrent posterior aortopexy, hospitalizations malrotation, intubation respiratory ASD repair, revision for respiratory diaphragmatic infections posterior infections hernia tracheopexy, repair diaphragmatic hernia

ALTE = apneic apparent life-threatening event; ASD = atrial septal defect; AV = atrioventricular; BPD = bronchopulmonary dysplasia; BiPAP = bilevel positive airway pressure; CPAP = continuous positive airway pressure; DLB = diagnostic laryngoscopy and bronchoscopy; EA = esophageal atresia; FB = flexible bronchoscopy; L = left; LAD = large airway disease; LTR = laryngotracheal reconstruction; NA = not available; PA = pulmonary artery; PDA = patent ductus arteriosus; PEEP = positive end-expiratory pressure; PFO = patent foramen ovale; pHTN = pulmonary hypertension; PPV = positive pressure ventilation; PV = pulmonary valve; R = right; SGS = subglottic stenosis; TBM = tracheobronchomalacia; TEF = tracheoesophageal fistula; TOF = tetralogy of Fallot; Trach = tracheostomy; TVC = true vocal cord; VSD = ventricular septal defect; WOB = work of breathing. surgery, and posterior tracheopexy will follow at a later date for new tracheotomy was performed in two patients for bilateral persistent symptoms and signs of TBMondynamicbronchoscopy. vocal-fold immobility; both still needed intermittent PPV, At our institution, close to 300 patients have undergone although the settings were improved. One patient developed posterior tracheopexy for severe TBM. The 25 patients reported temporary vocal-fold immobility that resolved without inter- in this series represent the only patients to have undergone both vention. One patient had a chyle leak that was treated non- anterior and posterior tracheopexy. operatively. There were no postoperative deaths. Identification and repair of synchronous airway lesions was performed by pediatric otolaryngologists. Three patients RESULTS had true vocal-fold weaknesses diagnosed preoperatively, all Twenty-five patients underwent anterior and poste- unilateral left cord, presumed to have been caused by prior rior tracheopexy at a mean age of 15.8 months (range, cardiac or EA surgeries. The one patient with synchronous 2–209 months; mean, 31 months if 2 outliers of 206 and laryngomalacia required a supraglottoplasty. Laryngeal cleft 209 months are included). Mean length of follow-up was was identified but not repaired in two of seven patients 26.8 months (range, 14–52 months). Surgical indica- (29%; 1 type 1, 1 type 2). Cleft repairs were performed in five tions were often multifactorial and are presented in of seven patients diagnosed with laryngeal cleft (50%; 1 type Table I. Many patients had other underlying syndromes 1, 3 type 2, and 1 type 3). All cleft repairs were performed and synchronous upper aerodigestive tract lesions endoscopically. One patient had concurrent subglottic steno- (Table II). Patient characteristics, including comorbidities, sis; one required laryngotracheal reconstruction before preoperative indications, procedures, and outcomes can be decannulation following surgery for TBM. found in Table III. Three patients with preoperative vocal- fold immobilities were identified, although these were likely related to prior surgeries at outside institutions. DISCUSSION The status of vocal-fold mobility was unknown preopera- It is important that the otolaryngologist is familiar with tively in five patients. the diagnosis and treatment of TBM, as presenting com- All patients underwent pre- and postoperative bron- plaints of cough, expiratory stridor, cyanotic/apneic episodes, choscopy. At preoperative bronchoscopy, 21 of 25 patients and recurrent or prolonged respiratory infections often had a complete collapse of at least one segment of their prompt otolaryngology referrals. Direct tracheobronchoscopy trachea, and the remaining four had 70% to 90% collapse. is the gold standard for diagnosis of TBM, but we advocate for Anterior and posterior tracheopexy was performed during the use of dynamic three-phase bronchoscopy to facilitate clas- the same operation in nine of 25 patients (36%) during car- sification and to diagnose dynamic collapse, TEF, or tracheal diac surgery. Posterior tracheopexy was performed first, diverticula that may be missed during a static shallow- followed by anterior tracheopexy at a later date in 12 of breathing evaluation. TBM is often associated with synchro- 25 patients (48%). Anterior tracheopexy was performed dur- nous airway lesions and should be considered during direct ing cardiac surgery and preceding posterior tracheopexy in laryngoscopies and bronchoscopies performed on children four of 25 patients (16%). When the two procedures were with airway symptoms.1,2,5–7 The strongest association not performed during the same operation, the mean opera- appears to exist between TBM and EA/TEF and tracheal tive interval was 184 days (range, 15–1,138 days). Concur- diverticulum.2,15 Synchronous laryngomalacia, laryngeal rent aortopexy was performed in 19 of 25 patients (76%). All cleft, vocal-fold immobility, and subglottic stenosis have six patients that did not undergo aortopexy had aortic arch also been reported.5–7 anomalies. Two of these patients had simultaneous thoracot- Otolaryngologists are critical members of multi- omy with posterior tracheopexy and then sternotomy with disciplinary teams that care for patients with TBM. The anterior tracheopexy, which was reserved for those patients role of the otolaryngologist includes performing flexible who had insufficient improvement on intraoperative bron- laryngoscopies to evaluate pre- and postoperative vocal-fold choscopy after posterior tracheopexy. mobility and direct laryngoscopies and bronchoscopies to Postoperatively, most patients had significant im- diagnose TBM and synchronous lesions and functioning as a provement in their preoperative respiratory symptoms member of the surgical team when addressing TBM. When (21 of 25, 84%) at most recent follow-up; specific outcomes pediatric otolaryngologists diagnose TBM, it is important to for each patient can be found in Table III. Decannulation be able to discuss the treatment options available for the was achieved in three patients with preexisting tracheot- patient. The association of synchronous airway disease in omy; two patients still had a tracheotomy at last follow-up our cohort, including subglottic stenosis and laryngomalacia, for continued airway small collapse (lobar and segmental), underscores the importance of involving otolaryngologists in chronic lung disease, and ventilator requirements related the care of these complex patients. to complications of anoxic brain injury. Following anterior A Cochrane review of interventions for pediatric and posterior tracheopexy, one patient developed new bilat- TBM, performed before these techniques were developed, eral vocal-fold immobility; one patient with a preoperative showed a dearth of quality evidence to support any means left cord paralysis had a new right vocal-fold immobility. of treatment.17 Today’s surgeons treating TBM have Both patients with new vocal-fold immobilities underwent many new techniques in their arsenal, and each patient’s simultaneous, challenging EA/TEF revisions after a pri- unique presentation should guide treatment and surgical mary repair at an outside institution; the patient that approach. We compare our innovative procedures to the developed a new right vocal-fold immobility also underwent most commonly reported techniques. When posterior simultaneous double aortic arch repair. Postoperatively, tracheopexy was first described by our group, of the nine

Laryngoscope 130: February 2020 Lawlor et al.: Tracheopexy for Severe Tracheobronchomalacia E72 patients that had preoperative tracheotomies, only two normal preoperative function. Postoperative new vocal could be decannulated after posterior tracheopexy. Statis- fold immobility was identified in two of our patients tically significant improvements in respiratory symptoms (1 bilateral and 1 unilateral coupled with preoperative were reported without data.15 However, with more expe- contralateral paralysis, resulting in bilateral immobility), rience, we have documented significant improvement in resulting in new postoperative tracheotomy placement. TBM with posterior tracheal procedures in isolation.18,19 This underscores the important role of otolaryngology In 2017, Morrison et al. described their 10-year experience in the preoperative planning, specifically to perform preop- treating severe TBM with aortopexies, intraluminal stents, erative flexible laryngoscopic evaluation and direct la- and tracheotomies; improvement in respiratory symptoms ryngoscopy and bronchoscopy to assess for synchronous was reported in 75%, 81%, and 67% of patients, respec- airway lesions. tively. Severe complications, including chylothorax, trache- Our patient with postoperative temporary vocal fold ostomy plugging, and stent fracture, occurred in 12%, 24%, paresis underscores the need for close otolaryngology and 33%, respectively.20 Anterior aortopexy, a procedure follow-up in these patients. Both patients with new vocal commonly utilized to treat TBM, has documented success fold immobility had complex congenital anomalies. Those rates from 60% to 100% and is also not without risk. Com- patients underwent simultaneous revision EA/TEF repair plications can occur in as many as 16% of patients, includ- after a prior repair had been performed at an outside ing pneumothorax, pericardial effusion, phrenic nerve institution. Revision EA/TEF repairs can be very techni- injury, and death.21,22 Injury to the RLN, despite an inci- cally challenging, with extensive infection, inflammation, dence of approximately 1% after thoracic surgery, is not and scar in the tracheoesophageal grooves. One of the commonly documented in the TBM literature.23 patients also had a concurrent double aortic arch repair. In this article, we describe a novel surgical technique These procedures also place the RLN at risk for injury. in the management of TBM: combined anterior and poste- Complex procedures in the neck and mediastinum do rior tracheobronchopexy. In our 25-patient cohort, 84% of place the RLN at risk for temporary or permanent injury. patients experienced improvement in their preoperative In retrospect, it is impossible to identify where and when respiratory symptoms. Patients with severe TBM that during those technically challenging multilevel surgeries requires anterior and posterior tracheopexy are usually the RLNs were injured. Our team is actively pursuing complex and may have comorbid respiratory diseases, methods to protect and/or intraoperatively monitor the such has bronchomalacia, bronchopulmonary dysplasia, RLNs during these procedures. We also acknowledge that and chronic lung disease. These illnesses can confound this potential morbidity is crucial to discuss during the postoperative evaluation of improvement in respiratory consent process prior to performing these procedures. symptoms. Thus, we considered our surgeries successful Otolaryngologists play a vital role in the management of if our patients had significant improvement or resolution this complication, with tracheotomies and vocal fold of their surgical indications, such as resolution in apneic medializations as indicated. spells or weaning off PPV. Of the five patients who required Limitations of this report include the small size of preoperative tracheotomy for respiratory support, three the cohort. As this procedure is relatively new, our lon- were decannulated during the period of documented follow- gitudinal data collection on patients is relatively short. up. One of those patients had severe subglottic stenosis Outcome measures such as improvement in respiratory and required a laryngotracheal reconstruction prior to de- symptoms can be subjective and dependent on length of cannulation. Two patients were unable to be decannulated; follow-up, although resolution of need for PPV or sup- both continued to require PPV. Both of those patients had plemental oxygen, repeated hospitalizations, tracheot- lower ventilator pressures, but severe chronic lung disease omy decannulation, and CPAP settings do provide some or distal small airway bronchomalacia required continued objective data. Further investigation into means of ventilator support. Symptoms did not improve in four of protecting the RLN is vital to the success of these tech- 25 (16%) patients when compared to their preoperative com- nically challenging procedures. This report is not meant plaints. Two of the patients considered failures were those to be a comment on the efficacy of anterior or posterior unable to be decannulated; it should be noted that their tracheopexy procedures in isolation; outcomes of poste- chronic lung disease may confound ventilator weaning. The rior tracheopexy have been published and are continu- other two patients were those who had tracheotomy placed ally reassessed.12–15,18,19 Finally, this article represents after anterior and posterior tracheopexy for bilateral true the outcomes from a single center. vocal fold immobility; both of those patients continued to require intermittent PPV. Anterior and posterior tracheopexy is an extensive CONCLUSION surgery and is not without morbidity. All patients in our This is the first report of a novel surgical approach cohort are still living. Due to the extensive anterior and to TBM: anterior and posterior tracheopexy. Our early posterior tracheal dissection, a vexing potential postopera- surgical outcomes are promising, with most patients re- tive complication is new unilateral or bilateral true vocal porting improvement in preoperative respiratory symptoms. fold immobility or paralysis that may significantly worsen The RLN is at risk during extensive paratracheal dissection, a tenuous patient’s respiratory status. Unfortunately, and true vocal fold immobility was a complication noted in despite many of our patients having had prior surgery, our cohort. The otolaryngologist plays a crucial role in the flexible laryngoscopy to assess vocal fold mobility preoper- treatment of TBM, particularly in pre- and postoperative atively was not performed on all patients to document evaluation and assistance.

Laryngoscope 130: February 2020 Lawlor et al.: Tracheopexy for Severe Tracheobronchomalacia E73 BIBLIOGRAPHY 14. Bairdain S, Smithers CJ, Hamilton TE, et al. Direct tracheobronchopexy to correct airway collapse due to severe tracheobronchomalacia: short- 1. Carden KA, Boiselle PM, Waltz DA, et al. Tracheomalacia and term outcomes in a series of 20 patients. J Pediatr Surg 2015;50: tracheobronchomalacia in children and adults. Chest 2006;127:964–1005. 972–977. 2. Fraga JC, Jennings RW, Kim PCW. Pediatric tracheomalacia. Semin 15. Shieh HF, Smithers CJ, Hamilton TE, et al. Posterior tracheopexy for Pediatr Surg 2016;25:156–164. severe tracheomalacia. J Pediatr Surg 2017;52:951–955. 3. Hammond K, Ghori U, Musani A. Tracheobronchomalacia and excessive 16. Propst EJ, Zawawi F, Kirsch RE, Honjo O. Direct tracheobronchopexy via dynamic airway collapse. Clin Chest Med 2018;39:223–228. left lateral thoracotomy for severe tracheobronchomalacia. Int J Pediatr 4. Rogers DJ, Cunnane MB, Hartnick CJ. Vascular compression of the airway. Otorhinolaryngol 2017;103:32–35. JAMA Otolaryngol Head Neck Surg 2013;139:586–591. 17. Goyal V, Masters IB, Chang AB. Interventions for primary (intrinsic) 5. Hseu A, Recko T, Jennings R, Nuss R. Upper airway anomalies in congeni- tracheomalacia in children. Cochrane Database Syst Rev 2012;10: tal tracheoesophageal fistula and esophageal atresia patients. Ann Otol CD005304. Rhinol Laryngol 2015;124:808–813. 18. Shieh HF, Smithers CJ, Hamilton TE, et al. Descending aortopexy and pos- 6. Londahl M, Irace AL, Kawai K, Dombrowski ND, Jennings R, Rahbar R. terior tracheopexy for severe tracheomalacia and left mainstem Prevalence of laryngeal cleft in pediatric patients with esophageal atresia. bronchomalacia [published online March 7, 2018]. Semin Thorac Cardi- JAMA Otolaryngol Head Neck Surg 2018;144:164–168. ovasc Surg doi: https://doi.org/10.1053/j.semtcvs.2018.02.031. 7. Fraga JC, Adil EA, Kacprowicz A, et al. The association between laryngeal 19. Shieh HF, Smithers CJ, Hamilton TE, et al. Posterior tracheopexy for cleft and tracheoesophageal fistula: myth or reality? Laryngoscope 2015; severe tracheomalacia associated with esophageal atresia (EA): primary 125:469–474. treatment at the time of initial EA repair versus secondary treatment. 8. Filler RM, Fraga JC. Tracheomalacia. Semin Thorac Cardiovasc Surg 1994; Front Surg 2018;4:80. 6:211–215. 20. Morrison RJ, Sengupta S, Flanangan CL, Ohye RG, Hollister SJ, Green GE. 9. Deacon JWF, Widger J, Soma MA. Paediatric tracheomalacia - a review of Treatment of severe acquired tracheomalacia with a patient-specific, 3D- clinical features and comparison of diagnostic imaging techniques. Int J printed, permanent tracheal splint. JAMA Otolaryngol Head Neck Surg Pediatr Otorhinolaryngol 2017;98:75–81. 2017;143:523–525. 10. Jacobs IN, Wetmore RF, Handler SD, et al. Tracheobronchomalacia in chil- 21. Jennings RW, Hamilton TE, Smithers CJ, Ngerncham M, Feins N, dren. Arch Otol Head Neck Surg 1994;120:154–158. Foker JE. Surgical approaches to aortopexy for severe tracheomalacia. 11. Benjamin B, Cohen D, Glasson M. Tracheomalacia in association with con- J Pediatr Surg 2014;49:66–70; discussion 70–71. genital tracheoesophageal fistula. Surgery 1976;79:504–508. 22. Torre M, Carlucci M, Speggiorin S, Elliott MJ. Aortopexy for the treatment 12. Bairdain S, Zurakowski D, Baird CW, Jennings RW. Surgical treatment of of tracheomalacia in children: review of the literature. Ital J Pediatr 2012; tracheobronchomalacia: a novel approach. Paediatr Respir Rev 2016;19:16–20. 38:62. 13. de Trey LA, Dudley J, Ismail-Koch H, et al. Treatment of severe 23. Krasna MJ, Forti G. Nerve injury: injury to the recurrent laryngeal, tracheobronchomalacia: ten-year experience. Int J Pediatr Otorhinolaryngol phrenic, vagus, long thoracic, and sympathetic nerves during thoracic sur- 2016;83:57–62. gery. Thorac Surg Clin 2006;16:267–275, vi.

Laryngoscope 130: February 2020 Lawlor et al.: Tracheopexy for Severe Tracheobronchomalacia E74