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Longitudinal Follow-up of Chronic Pulmonary Manifestations in Esophageal Atresia: A Clinical Algorithm and Review of the Literature

Open AccessPublished:June 18, 2016DOI:https://doi.org/10.1016/j.pedneo.2016.03.005
      In the past decades improved surgical techniques and better neonatal supportive care have resulted in reduced mortality of patients with esophageal atresia (EA), with or without tracheoesophageal fistula, and in increased prevalence of long-term complications, especially respiratory manifestations. This integrative review describes the techniques currently used in the pediatric clinical practice for assessing EA-related respiratory disease. We also present a novel algorithm for the evaluation and surveillance of lung disease in EA. A total of 2813 articles were identified, of which 1451 duplicates were removed, and 1330 were excluded based on review of titles and abstracts. A total of 32 articles were assessed for eligibility. Six reviews were excluded, and 26 original studies were assessed. Lower respiratory tract infection seems frequent, especially in the first years of life. Chronic asthma, productive cough, and recurrent bronchitis are the most common respiratory complaints. Restrictive lung disease is generally reported to prevail over the obstructive or mixed patterns, and, overall, bronchial hyperresponsiveness can affect up to 78% of patients. At lung imaging, few studies detected bronchiectasis and irregular cross-sectional shape of the trachea, whereas diffuse bronchial thickening, consolidations, and pleural abnormalities were the main chest X-ray findings. Airway endoscopy is seldom included in the available studies, with tracheomalacia and tracheobronchial inflammation being described in a variable proportion of cases. A complete diagnostic approach to long-term respiratory complications after EA is mandatory. In the presence of moderate-to-severe airway disease, patients should undergo regular tertiary care follow-up with functional assessment and advanced chest imaging.

      Key Words

      1. Introduction

      Esophageal atresia (EA) with or without tracheoesophageal fistula (TEF) occurs in one per 3000 live births.
      • Kovesi T.
      • Rubin S.
      Long-term complications of congenital esophageal atresia and/or tracheoesophageal fistula.
      • Fragoso A.C.
      • Tovar J.A.
      The multifactorial origin of respiratory morbidity in patients surviving neonatal repair of esophageal atresia.
      • Kovesi T.
      Long-term respiratory complications of congenital esophageal atresia with or without tracheoesophageal fistula: An update.
      In recent decades, improved surgical techniques and better neonatal supportive care have resulted in reduced mortality and increased prevalence of long-term disease-related complications, the most frequent of which include respiratory manifestations.
      • Castilloux J.
      • Noble A.J.
      • Faure C.
      Risk factors for short- and long-term morbidity in children with esophageal atresia.
      Recurrent-to-chronic respiratory symptoms may upset daily life of EA survivors,
      • Delacourt C.
      • de Blic J.
      Pulmonary outcome of esophageal atresia.
      and this is the reason why the assessment of pulmonary disease is recommended in these patients. This integrative review describes the various techniques currently used in pediatric clinical practice for assessing EA-related respiratory disease. Moreover, we present a novel algorithm for the evaluation and surveillance of lung disease in EA survivors. We carried out an electronic keyword literature search for English articles published on this topic up to September 22, 2015, in the Scopus, Web of Science, PubMed, and MEDLINE databases. We excluded the studies conducted exclusively on adults, but included those with a study population comprising children (or adolescents) and adults. The terms “esophageal atresia” AND (lung OR respiratory OR pulmonary OR airway or spirometry or complications or diagnostic tools) were used as keywords in combination, and the studies found were evaluated for selecting relevant literature. In addition, a manual search was conducted to evaluate review articles' references. Literature reviews on diagnostic procedures for EA-related pulmonary disease prompted us to develop a novel algorithm for the evaluation and surveillance of lung disease in EA survivors.

      2. Etiology

      The etiology of pulmonary manifestations following EA repair is multifaceted. Because newborns with EA have an increased risk of premature birth that may initiate the clinical scenario,
      • Gibson A.M.
      • Doyle L.W.
      Respiratory outcomes for the tiniest or most immature infants.
      the association with anomalies such as tracheomalacia and lung hypoplasia may significantly contribute to respiratory morbidity since birth.
      • Fragoso A.C.
      • Tovar J.A.
      The multifactorial origin of respiratory morbidity in patients surviving neonatal repair of esophageal atresia.
      Gastrointestinal symptoms (i.e., regurgitation and/or feeding difficulties with repetitive cough during swallowing, and/or dysphagia and heartburn likely due to peptic esophagitis and Barrett's esophagus) represent the major complaints at any age, and an association of gastrointestinal and respiratory symptoms has been hypothesized to imply a correlation between esophageal and lung dysfunction.
      • Kovesi T.
      • Rubin S.
      Long-term complications of congenital esophageal atresia and/or tracheoesophageal fistula.
      • Delacourt C.
      • de Blic J.
      Pulmonary outcome of esophageal atresia.
      • Faure C.
      Endoscopic features in esophageal atresia: From birth to adulthood.
      Indeed, esophageal dysmotility and gastroesophageal reflux (GER) may cause and/or worsen wheezing, bronchial asthma, and pneumonia.
      • Peetsold M.G.
      • Heij H.A.
      • Nagelkerke A.F.
      • Deurloo J.A.
      • Gemke R.J.
      Pulmonary function impairment after trachea-esophageal fistula: A minor role for gastro-esophageal reflux disease.
      Although the underlying mechanisms are still being debated, literature suggests that chronic asthma is likely elicited by a reflex mechanism and that recurrent pneumonia may be explained by repetitive acid aspiration.
      • Cucchiara S.
      • Santamaria F.
      • Minella R.
      • Alfieri E.
      • Scoppa A.
      • Calabrese F.
      • et al.
      Simultaneous prolonged recordings of proximal and distal intraesophageal pH in children with gastroesophageal reflux disease and respiratory symptoms.
      • Berquist W.E.
      • Rachelefsky G.S.
      • Kadden M.
      • Siegel S.C.
      • Katz R.M.
      • Fonkalsrud E.W.
      • et al.
      Gastroesophageal reflux-associated recurrent pneumonia and chronic asthma in children.
      Chronic airway inflammation with bouts of infection can eventually result in segmental or even lobar damage leading to the development of severe, life-threatening lung disease in a proportion of patients.
      • Chetcuti P.
      • Phelan P.D.
      Respiratory morbidity after repair of oesophageal atresia and tracheo-oesophageal fistula.
      • Malmström K.
      • Lohi J.
      • Lindahl H.
      • Pelkonen A.
      • Kajosaari M.
      • Sarna S.
      • et al.
      Longitudinal follow-up of bronchial inflammation, respiratory symptoms, and pulmonary function in adolescents after repair of esophageal atresia with tracheoesophageal fistula.
      • Sarnelli P.
      • Cucchiara S.
      • Celentano L.
      • Settimi A.
      • Tramontano A.
      • Barbarano F.
      • et al.
      Pulmonary manifestations following esophageal atresia repair: A case series.
      • Choudhury S.R.
      • Ashcraft K.W.
      • Sharp R.J.
      • Murphy J.P.
      • Snyder C.L.
      • Sigalet D.L.
      Survival of patients with esophageal atresia: Influence of birth weight, cardiac anomaly, and late respiratory complications.
      Finally, recurrent TEF may further complicate the clinical course.
      • Rintala R.J.
      • Sistonen S.
      • Pakarinen M.P.
      Outcome of esophageal atresia beyond childhood.
      Following EA-TEF repair, structural anomalies persist in both the trachea and the esophagus, and chest wall deformities, exacerbated by thoracotomy, may further contribute to alter pulmonary function.
      • Fragoso A.C.
      • Tovar J.A.
      The multifactorial origin of respiratory morbidity in patients surviving neonatal repair of esophageal atresia.

      3. Respiratory complications

      Patients with EA with or without TEF experience respiratory complaints more often and more persistently than other individuals, and recurrent bronchitis, chronic cough, repeated pneumonia, and asthma-like wheezing represent the major clinical manifestations.
      • Chetcuti P.
      • Phelan P.D.
      Respiratory morbidity after repair of oesophageal atresia and tracheo-oesophageal fistula.
      • Sulkowski J.P.
      • Cooper J.N.
      • Lopez J.J.
      • Jadcherla Y.
      • Cuenot A.
      • Mattei P.
      • et al.
      Morbidity and mortality in patients with esophageal atresia.
      Lower respiratory tract infection is abnormally common especially in the first years of life, with more than five annual respiratory tract infections and a rate of more than three attacks of bronchitis per year of up to 78%.
      • Gischler S.J.
      • van der Cammen-van Zijp M.H.
      • Mazer P.
      • Madern G.C.
      • Bax N.M.
      • de Jongste J.C.
      • et al.
      A prospective comparative evaluation of persistent respiratory morbidity in esophageal atresia and congenital diaphragmatic hernia survivors.
      • Dudley N.E.
      • Phelan P.D.
      Respiratory complications in long-term survivors of oesophageal atresia.
      In a study from Finland, aspiration pneumonia likely related to impaired esophageal peristalsis and esophageal stricture was reported in approximately 50% of affected children, although they did not experience more current respiratory or esophageal symptoms than those without.
      • Malmström K.
      • Lohi J.
      • Lindahl H.
      • Pelkonen A.
      • Kajosaari M.
      • Sarna S.
      • et al.
      Longitudinal follow-up of bronchial inflammation, respiratory symptoms, and pulmonary function in adolescents after repair of esophageal atresia with tracheoesophageal fistula.
      Coughs with sputum production and recurrent bronchitis are significantly more common among patients with repaired EA than among healthy individuals,
      • Gatzinsky V.
      • Jönsson L.
      • Ekerljung L.
      • Friberg L.G.
      • Wennergren G.
      Long-term respiratory symptoms following oesophageal atresia.
      and although respiratory morbidity tends to improve with age, chronic cough, associated with bronchial constriction and hyperresponsiveness, can persist or even become more frequent in adulthood.
      • Gatzinsky V.
      • Wennergren G.
      • Jönsson L.
      • Ekerljung L.
      • Houltz B.
      • Redfors S.
      • et al.
      Impaired peripheral airway function in adults following repair of esophageal atresia.
      As a consequence of repeated bouts of lower airways infection, bronchiectasis may also develop.
      • Banjar H.
      Bronchiectasis following repair of esophageal atresia and tracheo-esophageal fistula.
      Although some respiratory complications may be accounted for by documented tracheomalacia, esophageal dysmotility, GER disease (GERD), or surgical complications, a high proportion of EA survivors have abnormal pulmonary function that is apparently unrelated to these conditions.
      • Fragoso A.C.
      • Tovar J.A.
      The multifactorial origin of respiratory morbidity in patients surviving neonatal repair of esophageal atresia.
      A restrictive pattern generally prevailing over obstructive or restrictive-obstructive airway disease has been described in up to 96% of children, adolescents, and adults previously treated for EA with or without TEF.
      • Kovesi T.
      • Rubin S.
      Long-term complications of congenital esophageal atresia and/or tracheoesophageal fistula.
      • Malmström K.
      • Lohi J.
      • Lindahl H.
      • Pelkonen A.
      • Kajosaari M.
      • Sarna S.
      • et al.
      Longitudinal follow-up of bronchial inflammation, respiratory symptoms, and pulmonary function in adolescents after repair of esophageal atresia with tracheoesophageal fistula.
      • Milligan D.W.
      • Levison H.
      Lung function in children following repair of tracheoesophageal fistula.
      • Legrand C.
      • Michaud L.
      • Salleron J.
      • Neut D.
      • Sfeir R.
      • Thumerelle C.
      • et al.
      Long-term outcome of children with oesophageal atresia type III.
      • Beucher J.
      • Wagnon J.
      • Daniel V.
      • Habonimana E.
      • Fremond B.
      • Lapostolle C.
      • et al.
      Long-term evaluation of respiratory status after esophageal atresia repair.
      Interestingly, approximately one-third of a Finnish pediatric population had restrictive or obstructive defects that were apparently unrelated to current respiratory or esophageal symptoms.
      • Malmström K.
      • Lohi J.
      • Lindahl H.
      • Pelkonen A.
      • Kajosaari M.
      • Sarna S.
      • et al.
      Longitudinal follow-up of bronchial inflammation, respiratory symptoms, and pulmonary function in adolescents after repair of esophageal atresia with tracheoesophageal fistula.
      In the same study, bronchial hyperresponsiveness was found to be severe/moderate or mild in 26% or 52% of the cases, respectively. Airflow obstruction may be explained by several mechanisms including small airway disease or proximal obstruction due to airway malacia or epithelial damage caused by GERD and recurrent episodes of bronchitis or aspiration pneumonia worsened by poor tracheal clearance, or decreased lung growth during infancy.
      • LeSouëf P.N.
      • Myers N.A.
      • Landau L.I.
      Etiologic factors in long-term respiratory function abnormalities following esophageal atresia repair.
      Multiple potential predisposing factors to restrictive lung disease are also congenital or acquired vertebral or chest wall abnormalities (i.e., scoliosis or postoperative rib fusions), surgical trauma, aspiration, and/or recurrent chest infections.
      • Kovesi T.
      • Rubin S.
      Long-term complications of congenital esophageal atresia and/or tracheoesophageal fistula.
      Chronic asthma is considered to be common in EA survivors, with significant bronchial inflammation also occurring in patients with nonallergic asthma.
      • Sarnelli P.
      • Cucchiara S.
      • Celentano L.
      • Settimi A.
      • Tramontano A.
      • Barbarano F.
      • et al.
      Pulmonary manifestations following esophageal atresia repair: A case series.
      • Agrawal L.
      • Beardsmore C.S.
      • MacFadyen U.M.
      Respiratory function in childhood following repair of oesophageal atresia and tracheoesophageal fistula.
      Whatever the initial trigger is, asthma significantly contributes to respiratory morbidity in EA, and it might even worsen pre-existing GERD.
      • Sarnelli P.
      • Cucchiara S.
      • Celentano L.
      • Settimi A.
      • Tramontano A.
      • Barbarano F.
      • et al.
      Pulmonary manifestations following esophageal atresia repair: A case series.

      4. Management

      With improved patient survival due to better neonatal care and surgery, the importance of recognition and management of pulmonary disease has increased. Table 1 summarizes the main findings from 26 original articles that exclusively investigated respiratory disease in EA survivors.
      Table 1Main findings from the 26 original articles that exclusively investigated respiratory disease in esophageal atresia survivors.
      StudyAge (y)Lung imagingPulmonary function testsBronchoscopyOtherMain findings
      Dudley & Phelan
      • Dudley N.E.
      • Phelan P.D.
      Respiratory complications in long-term survivors of oesophageal atresia.
      1 to >9Clinical outcomeRecurrent bronchitis during the first 3 y (78%)
      Milligan & Levison
      • Milligan D.W.
      • Levison H.
      Lung function in children following repair of tracheoesophageal fistula.
      7–18Spirometry

      MCT
      Obstructive (54%) & restrictive (21%) lung diseases

      Bronchial hyperreactivity (65%)
      Couriel et al
      • Couriel J.M.
      • Hibbert M.
      • Olinsky A.
      • Phelan P.D.
      Long term pulmonary consequences of oesophageal atresia with tracheo-oesophageal fistula.
      8–17Spirometry

      MCT
      Clinical outcomeBronchitis for > 8 y (25%)

      Mild restrictive lung disease

      Bronchial hyperreactivity (22%)
      LeSouëf et al
      • LeSouëf P.N.
      • Myers N.A.
      • Landau L.I.
      Etiologic factors in long-term respiratory function abnormalities following esophageal atresia repair.
      12–21Spirometry

      Body plethysmography
      Significant reduction of lung volumes in the pneumonia group vs. the nonpneumonia group
      Chetcuti et al
      • Chetcuti P.
      • Myers N.A.
      • Phelan P.D.
      • Beasley S.W.
      Adults who survived repair of congenital oesophageal atresia and tracheo-oesophageal fistula.
      0–25Body plethysmographyDaily cough (15%), wheezing (40%), bronchitis (34%)

      RV increase (77%), significant reduction in VC & FEV1 in patients who wheezed in the past 12 mo
      Griscom & Martin
      • Griscom N.T.
      • Martin T.R.
      The trachea and esophagus after repair of esophageal atresia and distal fistula: Computed tomographic observations.
      2–21CTSpirometryBronchiectasis (40%)

      Mild restrictive (20%) & obstructive lung disease (40%)
      Chetcuti et al
      • Chetcuti P.
      • Phelan P.D.
      • Greenwood R.
      Lung function abnormalities in repaired oesophageal atresia and tracheo-oesophageal fistula.
      6–37Spirometry

      Body plethysmography
      Reduced FEV1 (25%) & RV/TLC ratio (41%)

      Restrictive lung disease (18%)
      Chetcuti & Phelan
      • Chetcuti P.
      • Phelan P.D.
      Respiratory morbidity after repair of oesophageal atresia and tracheo-oesophageal fistula.
      1–37Clinical outcomeIn the 0–5-y age group, pneumonia (50%), recurrent pneumonia (25%)

      Persistent cough (32% aged 0–5 y, 13% 5–10 y, 15% 10–15 y, & 9%>15 y)

      Typical harsh cough (71% aged 0–5 y, 60% 5–10 y, 57% 10–15 y, & 40%>15 y)
      Beardsmore et al
      • Beardsmore C.S.
      • MacFadyen U.M.
      • Johnstone M.S.
      • Williams A.
      • Simpson H.
      Clinical findings and respiratory function in infants following repair of oesophageal atresia and tracheo-oesophageal fistula.
      2–13 wkBody plethysmographyThoracic gas volume increase (33%), abnormalities in airway resistance pattern (78%), airway resistance increase (33%), limitation of inspiratory & expiratory airflow (11%)
      Montgomery et al
      • Montgomery M.
      • Frenckner B.
      • Freyschuss U.
      • Mortensson W.
      Esophageal atresia: Long-term-follow-up of respiratory function, maximal working capacity, and esophageal function.
      8–21Spirometry

      Body plethysmography

      Bicycle ergometer
      Clinical outcomeAsthma or bronchitis (39%)

      Obstructive (44%) & restrictive (55%) lung disease

      Decreased maximal working capacity (53%)
      Robertson et al
      • Robertson D.F.
      • Mobaireek K.
      • Davis G.M.
      • Coates A.L.
      Late pulmonary function following repair of tracheoesophageal fistula or esophageal atresia.
      7–28X-raySpirometry

      Body plethysmography

      MCT
      Clinical outcomeRespiratory symptoms (72%), bronchiectasis (4%), obstructive (12%), restrictive (36%), & mixed (4%) lung disease

      Positive MCT (24%)
      Somppi et al
      • Somppi E.
      • Tammela O.
      • Ruuska T.
      • Rahnasto J.
      • Laitinen J.
      • Turjanmaa V.
      • et al.
      Outcome of patients operated on for esophageal atresia: 30 years' experience.
      3.5–30SpirometryYesClinical outcomeReduced FEV1 (67%)

      Tracheal inflammation (37%). Respiratory infections (29%), recurrent dyspnea (28%), & cough during the night (37%)
      Agrawal et al
      • Agrawal L.
      • Beardsmore C.S.
      • MacFadyen U.M.
      Respiratory function in childhood following repair of oesophageal atresia and tracheoesophageal fistula.
      7–12Spirometry

      Body plethysmography
      Restrictive lung disease (67%)
      Choudhury et al
      • Choudhury S.R.
      • Ashcraft K.W.
      • Sharp R.J.
      • Murphy J.P.
      • Snyder C.L.
      • Sigalet D.L.
      Survival of patients with esophageal atresia: Influence of birth weight, cardiac anomaly, and late respiratory complications.
      0 d to >30 dClinical outcomeAspiration & pneumonia (13%) as early death causes

      Aspiration, tracheomalacia, & reactive airway disease as late death causes (59%)
      Soto et al
      • Soto M.C.
      • Rivilla F.
      • Dorado M.J.
      • Rueda S.
      • Balboa F.
      • Casillas J.G.
      Pneumopathy in patients surgically treated for type III esophageal atresia.
      1–15SpirometryRestrictive lung disease (50%)
      Little et al
      • Little D.C.
      • Rescorla F.J.
      • Grosfeld J.L.
      • West K.W.
      • Scherer L.R.
      • Engum S.A.
      Long-term analysis of children with esophageal atresia and tracheoesophageal fistula.
      18.7Clinical outcomeRespiratory infections (29%)
      Sarnelli et al
      • Sarnelli P.
      • Cucchiara S.
      • Celentano L.
      • Settimi A.
      • Tramontano A.
      • Barbarano F.
      • et al.
      Pulmonary manifestations following esophageal atresia repair: A case series.
      0.8–14.6X-ray

      HRCT

      Perfusion scintigraphy
      YesFamily history of atopy (40%) & allergic asthma (10%), lobar consolidations (80%), bronchiectasis (20%)
      Banjar
      • Banjar H.
      Bronchiectasis following repair of esophageal atresia and tracheo-esophageal fistula.
      1.25 ± 2.4CTSpirometry

      Body plethysmography
      Tracheomalacia (29%), bronchiectasis (17%), obstructive (7%), restrictive (20%), & mixed lung disease (7%)
      Lilja & Wester
      • Lilja H.E.
      • Wester T.
      Outcome in neonates with esophageal atresia treated over the last 20 years.
      1–20Clinical outcomeAt 16–20 y, frequent cough between (36%), impaired exercise capacity (20%), respiratory infections (40%), & shortness of breath (53%)
      Malmström et al
      • Malmström K.
      • Lohi J.
      • Lindahl H.
      • Pelkonen A.
      • Kajosaari M.
      • Sarna S.
      • et al.
      Longitudinal follow-up of bronchial inflammation, respiratory symptoms, and pulmonary function in adolescents after repair of esophageal atresia with tracheoesophageal fistula.
      9.7–19.4Spirometry

      Histamine challenge test
      YesFeNO, clinical outcomeObstructive (30%) & restrictive (35%) lung diseases

      Bronchial hyperreactivity (78%)

      Current respiratory symptoms (44%), wheezing (52%), pneumonia (52%)

      Mild (72%) & moderate bronchitis in biopsies (7%)

      Abnormal FeNO (23%)
      Gischler et al
      • Gischler S.J.
      • van der Cammen-van Zijp M.H.
      • Mazer P.
      • Madern G.C.
      • Bax N.M.
      • de Jongste J.C.
      • et al.
      A prospective comparative evaluation of persistent respiratory morbidity in esophageal atresia and congenital diaphragmatic hernia survivors.
      5–6.5Spirometry

      Treadmill test
      FeNO, clinical outcomeReduced FEV1 (25%)

      Abnormally low maximal exercise tolerance (6.3%)

      Normal FeNO

      High proportion of patients with >5 respiratory tract infections in 5 y (74%)
      Harrison et al
      • Harrison J.
      • Martin J.
      • Crameri J.
      • Robertson C.F.
      • Ranganathan S.C.
      Lung function in children with repaired tracheo-oesophageal fistula using the forced oscillation technique.
      7.6 ± 2.2Spirometry

      Forced oscillation technique

      Body plethysmography
      Reduced Rrs6 (27%) & Rrs8 (24%)

      FEV1 significantly lower in EA with TEF vs. healthy controls
      Peetsold et al
      • Peetsold M.G.
      • Heij H.A.
      • Nagelkerke A.F.
      • Deurloo J.A.
      • Gemke R.J.
      Pulmonary function impairment after trachea-esophageal fistula: A minor role for gastro-esophageal reflux disease.
      13.2 ± 2.9Spirometry

      Body plethysmography

      Cardiopulmonary exercise testing
      YesObstructive lung disease (13%)

      FVC & TLC significantly lower in EA with TEF vs. patients with gastroesophageal reflux disease
      Spoel et al
      • Spoel M.
      • Meeussen C.J.
      • Gischler S.J.
      • Hop W.C.
      • Bax N.M.
      • Wijnen R.M.
      • et al.
      Respiratory morbidity and growth after open thoracotomy or thoracoscopic repair of esophageal atresia.
      24–66 wkBody plethysmographyObstructive lung disease (19%)
      Legrand et al
      • Legrand C.
      • Michaud L.
      • Salleron J.
      • Neut D.
      • Sfeir R.
      • Thumerelle C.
      • et al.
      Long-term outcome of children with oesophageal atresia type III.
      13.3SpirometryClinical outcomeChronic cough (19%) & dyspnea (37%)

      Obstructive (50%) or restrictive (11%) lung disease
      Beucher et al
      • Beucher J.
      • Wagnon J.
      • Daniel V.
      • Habonimana E.
      • Fremond B.
      • Lapostolle C.
      • et al.
      Long-term evaluation of respiratory status after esophageal atresia repair.
      8.5X-raySpirometry

      MCT

      Bicycle ergometer
      Bilateral opacities, right lower lobe infiltrate, or pleural abnormalities (10%)

      Obstructive (19%) & restrictive (23%) lung disease

      Bronchial hyperreactivity (39%)

      Reduced ventilation reserve (45%)
      CT = computed tomography; EA = esophageal atresia; FeNO = fractional concentration of exhaled nitric oxide; FEV1 = forced expiratory volume in one second; FVC = forced vital capacity; HRCT = high-resolution computed tomography; MCT = methacholine challenge test; Rrs6 = resistance at 6 Hz; Rrs8 = resistance at 8 Hz; RV = residual volume; TEF = tracheoesophageal fistula; TLC = total lung capacity; VC = vital capacity.
      Several studies focused only on clinical outcomes,
      • Delius R.E.
      • Wheatley M.J.
      • Coran A.G.
      Etiology and management of respiratory complications after repair of esophageal atresia with tracheoesophageal fistula.
      • Little D.C.
      • Rescorla F.J.
      • Grosfeld J.L.
      • West K.W.
      • Scherer L.R.
      • Engum S.A.
      Long-term analysis of children with esophageal atresia and tracheoesophageal fistula.
      • Lilja H.E.
      • Wester T.
      Outcome in neonates with esophageal atresia treated over the last 20 years.
      whereas others also included functional assessment by spirometry,
      • Soto M.C.
      • Rivilla F.
      • Dorado M.J.
      • Rueda S.
      • Balboa F.
      • Casillas J.G.
      Pneumopathy in patients surgically treated for type III esophageal atresia.
      • Couriel J.M.
      • Hibbert M.
      • Olinsky A.
      • Phelan P.D.
      Long term pulmonary consequences of oesophageal atresia with tracheo-oesophageal fistula.
      • Chetcuti P.
      • Myers N.A.
      • Phelan P.D.
      • Beasley S.W.
      Adults who survived repair of congenital oesophageal atresia and tracheo-oesophageal fistula.
      • Chetcuti P.
      • Phelan P.D.
      • Greenwood R.
      Lung function abnormalities in repaired oesophageal atresia and tracheo-oesophageal fistula.
      • Montgomery M.
      • Frenckner B.
      • Freyschuss U.
      • Mortensson W.
      Esophageal atresia: Long-term-follow-up of respiratory function, maximal working capacity, and esophageal function.
      • Robertson D.F.
      • Mobaireek K.
      • Davis G.M.
      • Coates A.L.
      Late pulmonary function following repair of tracheoesophageal fistula or esophageal atresia.
      • Somppi E.
      • Tammela O.
      • Ruuska T.
      • Rahnasto J.
      • Laitinen J.
      • Turjanmaa V.
      • et al.
      Outcome of patients operated on for esophageal atresia: 30 years' experience.
      • Harrison J.
      • Martin J.
      • Crameri J.
      • Robertson C.F.
      • Ranganathan S.C.
      Lung function in children with repaired tracheo-oesophageal fistula using the forced oscillation technique.
      • Beardsmore C.S.
      • MacFadyen U.M.
      • Johnstone M.S.
      • Williams A.
      • Simpson H.
      Clinical findings and respiratory function in infants following repair of oesophageal atresia and tracheo-oesophageal fistula.
      airway challenge tests,
      • Malmström K.
      • Lohi J.
      • Lindahl H.
      • Pelkonen A.
      • Kajosaari M.
      • Sarna S.
      • et al.
      Longitudinal follow-up of bronchial inflammation, respiratory symptoms, and pulmonary function in adolescents after repair of esophageal atresia with tracheoesophageal fistula.
      • Beucher J.
      • Wagnon J.
      • Daniel V.
      • Habonimana E.
      • Fremond B.
      • Lapostolle C.
      • et al.
      Long-term evaluation of respiratory status after esophageal atresia repair.
      and/or lung volumes measurement.
      • Peetsold M.G.
      • Heij H.A.
      • Nagelkerke A.F.
      • Deurloo J.A.
      • Gemke R.J.
      Pulmonary function impairment after trachea-esophageal fistula: A minor role for gastro-esophageal reflux disease.
      • Spoel M.
      • Meeussen C.J.
      • Gischler S.J.
      • Hop W.C.
      • Bax N.M.
      • Wijnen R.M.
      • et al.
      Respiratory morbidity and growth after open thoracotomy or thoracoscopic repair of esophageal atresia.
      The restrictive pattern was generally reported to prevail over the obstructive or mixed ones, and, overall, bronchial hyperresponsiveness was found in up to 78% of patients.
      • Malmström K.
      • Lohi J.
      • Lindahl H.
      • Pelkonen A.
      • Kajosaari M.
      • Sarna S.
      • et al.
      Longitudinal follow-up of bronchial inflammation, respiratory symptoms, and pulmonary function in adolescents after repair of esophageal atresia with tracheoesophageal fistula.
      Of note, there were a few studies on chest imaging findings, which were reported in only five articles.
      • Sarnelli P.
      • Cucchiara S.
      • Celentano L.
      • Settimi A.
      • Tramontano A.
      • Barbarano F.
      • et al.
      Pulmonary manifestations following esophageal atresia repair: A case series.
      • Banjar H.
      Bronchiectasis following repair of esophageal atresia and tracheo-esophageal fistula.
      • Beucher J.
      • Wagnon J.
      • Daniel V.
      • Habonimana E.
      • Fremond B.
      • Lapostolle C.
      • et al.
      Long-term evaluation of respiratory status after esophageal atresia repair.
      • Robertson D.F.
      • Mobaireek K.
      • Davis G.M.
      • Coates A.L.
      Late pulmonary function following repair of tracheoesophageal fistula or esophageal atresia.
      • Griscom N.T.
      • Martin T.R.
      The trachea and esophagus after repair of esophageal atresia and distal fistula: Computed tomographic observations.
      In particular, three chest computed tomography (CT) studies detected bronchiectasis
      • Sarnelli P.
      • Cucchiara S.
      • Celentano L.
      • Settimi A.
      • Tramontano A.
      • Barbarano F.
      • et al.
      Pulmonary manifestations following esophageal atresia repair: A case series.
      • Griscom N.T.
      • Martin T.R.
      The trachea and esophagus after repair of esophageal atresia and distal fistula: Computed tomographic observations.
      and irregular cross-sectional shape of the trachea
      • Banjar H.
      Bronchiectasis following repair of esophageal atresia and tracheo-esophageal fistula.
      in a subgroup of patients, respectively. Chest CT findings may also include consolidations and/or bronchiectasis (Figure 1). By contrast, diffuse bronchial thickening, consolidations, and pleural abnormalities were the main chest X-ray findings described in a minority of patients.
      • Sarnelli P.
      • Cucchiara S.
      • Celentano L.
      • Settimi A.
      • Tramontano A.
      • Barbarano F.
      • et al.
      Pulmonary manifestations following esophageal atresia repair: A case series.
      • Beucher J.
      • Wagnon J.
      • Daniel V.
      • Habonimana E.
      • Fremond B.
      • Lapostolle C.
      • et al.
      Long-term evaluation of respiratory status after esophageal atresia repair.
      • Robertson D.F.
      • Mobaireek K.
      • Davis G.M.
      • Coates A.L.
      Late pulmonary function following repair of tracheoesophageal fistula or esophageal atresia.
      Airway endoscopy was seldom included in the available studies, with tracheomalacia representing a common finding
      • Peetsold M.G.
      • Heij H.A.
      • Nagelkerke A.F.
      • Deurloo J.A.
      • Gemke R.J.
      Pulmonary function impairment after trachea-esophageal fistula: A minor role for gastro-esophageal reflux disease.
      • Malmström K.
      • Lohi J.
      • Lindahl H.
      • Pelkonen A.
      • Kajosaari M.
      • Sarna S.
      • et al.
      Longitudinal follow-up of bronchial inflammation, respiratory symptoms, and pulmonary function in adolescents after repair of esophageal atresia with tracheoesophageal fistula.
      • Nasr A.
      • Ein S.H.
      • Gerstle J.T.
      Infants with repaired esophageal atresia and distal tracheoesophageal fistula with severe respiratory distress: Is it tracheomalacia, reflux, or both?.
      and tracheobronchial inflammation being described in a variable proportion of cases.
      • Malmström K.
      • Lohi J.
      • Lindahl H.
      • Pelkonen A.
      • Kajosaari M.
      • Sarna S.
      • et al.
      Longitudinal follow-up of bronchial inflammation, respiratory symptoms, and pulmonary function in adolescents after repair of esophageal atresia with tracheoesophageal fistula.
      • Somppi E.
      • Tammela O.
      • Ruuska T.
      • Rahnasto J.
      • Laitinen J.
      • Turjanmaa V.
      • et al.
      Outcome of patients operated on for esophageal atresia: 30 years' experience.
      In addition to tracheomalacia and bronchomalacia, less common anatomic abnormalities may include ectopic or absence of bronchus and congenital bronchial stenosis.
      • Kovesi T.
      • Rubin S.
      Long-term complications of congenital esophageal atresia and/or tracheoesophageal fistula.
      Undoubtedly, evaluation of the airways structure via flexible bronchoscopy can help identify these problems in infants and children before EA/TEF repair, or also in those with persistent respiratory symptoms after EA/TEF surgery.
      • Malmström K.
      • Lohi J.
      • Lindahl H.
      • Pelkonen A.
      • Kajosaari M.
      • Sarna S.
      • et al.
      Longitudinal follow-up of bronchial inflammation, respiratory symptoms, and pulmonary function in adolescents after repair of esophageal atresia with tracheoesophageal fistula.
      • Sarnelli P.
      • Cucchiara S.
      • Celentano L.
      • Settimi A.
      • Tramontano A.
      • Barbarano F.
      • et al.
      Pulmonary manifestations following esophageal atresia repair: A case series.
      Figure thumbnail gr1
      Figure 1Chest high-resolution computed tomography from two children with esophageal atresia and tracheoesophageal fistula repaired at birth and followed at our department: (A) left lower lobe consolidations and (B) left lower lobe consolidation with bronchiectasis.
      Although several articles on the main long-term respiratory complications in EA repair survivors have been published, a shared executive protocol has never been developed, nor have the available diagnostic tools been ordered in a management algorithm. Indeed, the few studies regarding the practical management of pulmonary complications in EA survivors and their heterogeneity make the development of an evidence-based operative algorithm virtually impossible. Nevertheless, due to the severe chronic complaints that some patients may experience and the impact on the healthcare costs, we propose a novel synthetic management algorithm (Figure 2), which may be helpful for clinicians dealing with lung disease secondary to EA. Basically, procedures are selected on the basis of the current clinical features. Present literature does not specify the timing of both follow-up visits and functional/chest imaging work-up. We suggest that basic procedures including transcutaneous pulse oximetry (SpO2), chest radiographs, and lung function tests (the latter only on cooperating patients) are at least obtained in all patients at baseline. We also propose that EA survivors, with or without TEF, should be differentiated between those with mild airway disease and those with moderate-to-severe airway disease. In particular, patients with respiratory symptoms (persistent cough, recurrent-to-persistent wheezing, recurrent respiratory infections) who show slight abnormalities or normal results of SpO2 at rest (ranging from 90% to 93%),
      • Balfour-Lynn I.M.
      • Field D.J.
      • Gringras P.
      • Hicks B.
      • Jardine E.
      • Jones R.C.
      • et al.
      BTS guidelines for home oxygen in children.
      • Aubertin G.
      • Marguet C.
      • Delacourt C.
      • Houdouin V.
      • Leclainche L.
      • Lubrano M.
      • et al.
      Recommendations for pediatric oxygen therapy in acute and chronic settings: Needs assessment, implementation criteria, prescription practices and follow-up.
      and/or chest radiography, and/or spirometry (i.e., forced expiratory volume in 1 second and forced vital capacity ≥ 70% predicted)
      • Miller M.R.
      • Hankinson J.
      • Brusasco V.
      • Burgos F.
      • Casaburi R.
      • Coates A.
      • et al.
      Standardisation of spirometry.
      are defined as having mild airway disease. Conversely, patients with respiratory symptoms and more relevant abnormalities of SpO2 at rest, and/or chest radiography, and/or spirometry are defined as having moderate-to-severe airway disease. We suggest that only the latter cases undergo regular tertiary care follow-up, including more extensive lung function assessment and advanced chest imaging (i.e., high-resolution CT and/or magnetic resonance imaging). A complete diagnostic approach to long-term respiratory complications after EA should also include tracheobronchial endoscopy with instillation of methylene blue for excluding recurrent TEF.
      • Delacourt C.
      • de Blic J.
      Pulmonary outcome of esophageal atresia.
      Recurrent TEF should be corrected using laparoscopic antireflux procedures to prevent lung damage.
      • Esposito C.
      • Langer J.C.
      • Schaarschmidt K.
      • Mattioli G.
      • Sauer C.
      • Centonze A.
      • et al.
      Laparoscopic antireflux procedures in the management of gastroesophageal reflux following esophageal atresia repair.
      • Wheatley M.J.
      • Coran A.G.
      • Wesley J.R.
      Efficacy of the Nissen fundoplication in the management of gastroesophageal reflux following esophageal atresia repair.
      These considerations lead to the conclusion that the evaluation of these patients is most efficiently accomplished in a tertiary care center where pediatric pulmonologists, gastroenterologists, radiologists, and surgeons are all available.
      Figure thumbnail gr2
      Figure 2Algorithm for the evaluation and surveillance of chronic pulmonary manifestations in esophageal atresia survivors with or without tracheoesophageal fistula. * To be obtained in all patients. FEV1 = forced expiratory volume in 1 second; FVC = forced vital capacity; SpO2 = arterial oxygen saturation measured by pulse oximetry.

      5. Conclusion

      In patients following EA repair, recurrent-to-persistent respiratory disease represents a major feature, especially in early to middle childhood.
      • Connor M.J.
      • Springford L.R.
      • Kapetanakis V.V.
      • Giuliani S.
      Esophageal atresia and transitional care—Step 1: A systematic review and meta-analysis of the literature to define the prevalence of chronic long-term problems.
      The persistence or recurrence of troublesome clinical manifestations imposes a scheduled follow-up of a large proportion of EA survivors, ideally through a multidisciplinary care approach for addressing their special needs. Pulmonary care of these patients involves managing comorbidities and preventing or minimizing damage to the lungs. Early detection and management of aspiration and other causes of recurrent-to-persistent lower airways infections in this population may be important to prevent decrements in pulmonary function and serious long-term complications.
      • Kovesi T.
      Long-term respiratory complications of congenital esophageal atresia with or without tracheoesophageal fistula: An update.
      A management algorithm for the evaluation and surveillance of EA-related respiratory disease based on the evidence from literature review is proposed. Like all algorithms, it is not meant to replace clinical judgment, but it should rather drive physicians to adopt a systematic approach to chronic pulmonary manifestations in EA survivors.

      Ethical statement

      This article does not contain any studies with human or animal subjects performed by any author(s).

      Conflicts of interest

      There are no financial or other relations that could lead to a conflicts of interest.

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