Gastroesophageal reflux disease (GERD) is common in children operated on at birth for esophageal atresia (EA). In this population, fundoplication has a high failure rate that was recently estimated to be 16%, the consequence of which was the need for subsequent reoperation (1). In 1997, Bianchi and colleagues described total esophagogastric disconnection (TED) as an alternative relevant surgical procedure to fundoplication for severe GERD in neurologically impaired children (2,3). This procedure was secondly used in patients with EA without neurological impairment (3,4). Short-term complications of TED (including acute hemorrhagic gastritis, subphrenic collection, esophagojejunal dehiscence, and small bowel hernia underneath the jejunal Roux loop) were first published in 2003 (5,6). Even if a 10-year review concluded that TED is a safe and effective procedure for GERD (6), long-term nutritional and metabolic complications have been reported in non-neurologic patients, including malabsorption, vitamin B12 deficiency, long-term dependency to enteral nutrition (EN), and dumping syndrome (7).
We report 2 severe, not yet described long-term complications of TED observed in children operated on at birth for EA.
Since 1999, 244 patients who underwent EA were studied at the Jeanne de Flandre Lille University Children's Hospital. During the same time period, 12 TEDs were performed: 5 in children with EA (severe GERD: n = 3; microgastria and GERD: n = 1; severe esophageal dyskinesia: n = 1), 6 in neurologically impaired children, and 1 in a child with laryngeal diastema. Four of the 5 children with EA presented the following complications: esophagojejunal anastomotic stricture (n = 1); Barrett esophagus (n = 1); combined esophagojejunal anastomotic stricture and gastric metaplasia (n = 2). Characteristics of the patients were retrospectively collected, including type of AE, surgical history, date of TED, date at first complication, and symptoms revealing complications, treatment, and outcome (Table 1).
A 5-year-old boy with type I EA had an end-to-end esophageal anastomosis at 4 months because of long-gap atresia. Despite a 5-month proton pump inhibitor (PPI) medication, GERD persisted. He underwent fundoplication at 9 months for severe GERD. Feeding difficulties and vomiting persisted in spite of a prolonged double-dose PPI medication, and a feeding gastrostomy was performed. Several months later, weaning from EN failed, and because of persisting vomiting and important oral disorders, he remained fed exclusively by a gastrojejunostomy. Because of persisting GERD symptoms in spite of exclusive EN and gastric feeding intolerance, an upper gastrointestinal x-ray was performed, showing a partially disrupted fundoplication and microgastria. Manometry showed severe dyskinesia. He underwent TED at 2 years. Vomiting disappeared but feeding difficulties persisted and oral feeding was still limited while he remained dependent on EN. At 3 years, he presented with aggravating feeding difficulties and salivary stasis. X-ray showed a stenosis of the esophagojejunal anatomosis (Fig. 1). A total of 8 endoscopic dilations using Savary-Gillard bougies (diameter 5–9 mm) were performed during a 2-year period, 2 of them being associated with mitomycin C application. With a follow-up of 7 months since the last dilation, he remained asymptomatic and stenosis did not recur. Repeated biopsies of the esophagojejunal anastomosis were normal, without inflammation and metaplasia.
An 11-year-old boy with type III EA was operated on at birth. Esophageal anastomotic stricture needed repeated dilations and feeding gastrostomy. Despite a 1-month double-dose PPI medication, GERD persisted and favored anastomotic stricture. He presented with several malaises caused by GERD and tracheomalacia. Because of this severe GERD favoring anastomotic stricture associated with microgastria, fundoplication was contraindicated and he underwent TED in first intention at the age of 1.5 months. From the age of 2 to 6 months, he underwent repeated endoscopy (n = 5) after TED for esophageal anastomotic surveillance and dilations (n = 5). No esophagojejunal anastomotic stenosis or Barrett was suspected. Dysphagia to solids and repeated food impactions occurred at the age of 9 years. X-ray showed incomplete esophagojejunal stenosis that was dilated with Savary-Gillard bougies (diameter 7–11 mm). Barrett esophagus was suspected starting from 15 cm under Killian upward to the esophagojejunal anastomosis. Histopathology confirmed gastric metaplasia of cardial type without intestinal metaplasia or dysplasia. Dysphagia improved without any treatment and food impactions did not recur. Endoscopy performed 2 years later showed no recurrence of esophagojejunal stenosis but persistence of Barrett of gastric type.
A 10-year-old boy was operated on at birth for type III EA. Because of a long gap and difficult anastomosis, gastric ascension was needed. One month later, revision of the ascended stomach was necessary for persistent feeding difficulties. Despite this second operation and the use of double-dose PPI treatment for 3 months, severe GERD persisted with gastric feeding intolerance leading to gastrojejunostomy feeding. One attempt at fundoplication failed because of microgastria and previous gastric operations. Severe acid GERD peristed at pH-metry, despite prolonged double-dose PPI medication, and the child presented repeated inhalation pneumonias making oral and enteral feeding impossible. TED was therefore performed at the age of 12 months. Twelve months after TED, he presented with worsened feeding difficulties, salivary stasis, and vomiting. An x-ray demonstrated moderate esophagojejunal stenosis. One balloon dilation (diameter 10–18 mm) was performed, and symptomatology improved thereafter. During follow-up, repeated endoscopy (n = 3) showed no recurrence of the stenosis or suspicion of Barrett. Nine years after TED, he presented with severe vomiting and dysphagia. Endoscopy showed no esophagojejunal stenosis but raised suspicions of the presence of Barrett esophagus extending 6 cm upward from the esophagojejunal junction (Fig. 2). Biopsies confirmed gastric metaplasia of cardiofundic type without intestinal metaplasia or dysplasia. PPIs treatment allowed dysphagia to improve. The child was doing well after a 3-month follow-up.
A 12-year-old boy was operated on at birth for type III EA. Because of severe GERD and dysphagia persisting despite long-term double-dose PPI treatment, he underwent fundoplication at 3 months complicated by mediastinitis and esophageal anastomotic stenosis that needed repeated endoscopic dilations (n = 6) with Savary-Gillard bougies (diameter 5–7 mm). GERD persisted despite antireflux surgery, prokinetics, and PPI. Endoscopy showed severe ulcerated esophagitis. Because of repeated respiratory failures and infections responsible for 3 hospitalizations in the intensive care unit, TED was performed at 14 months. The patient remained dependent on EN and presented severe dumping syndrome at 9 years. He regularly complained of dysphagia and food impactions. At 11.5 years, endoscopy showed a nodular aspect with hypervascularity and pseudopolyps around the esophagojejunal anastomosis. Histopathology confirmed gastric metaplasia of cardiofundic type without dysplasia. He remained asymptomatic and did not need any additional medication after an 18-month follow-up.
We are not aware of a previous description of esophagojejunal anastomotic stricture and gastric metaplasia as long-term complications of TED. TED is a recent surgical technique and the number of patients is limited; published series are small and follow-up is usually short (3,6,8). All patients with EA have a close follow-up in our reference center for congenital and malformative esophageal disorders. Endoscopy is frequently performed for symptoms or the survey of esophageal anastomosis and chronic esophagitis. This systematic follow-up obviously helps in the diagnosis of metaplasia and strictures, the symptoms of which are not specific, and can be absent or mild, or in relation to EA itself (ie, esophageal dysmotility) (9). In EA patients with TED, dysphagia can be related to many causes, including dumping syndrome, esophageal dysmotility, esophageal anastomotic stricture, or feeding disorders.
The reason for esophagojejunal stenosis in our patients is unclear. The role of surgery seems unlikely because no technical difficulty, anastomotic leakage, or mediastinitis occurred at the time of TED. Moreover, several patients had normal x-ray and/or endoscopy controls during the first year following TED. The abnormalities of distal esophageal tunica that have been described in EA (10) as well as severe acidic GERD may play a role in progressive anastomotic fibrosis. Bilious reflux is also a favoring cause of anastomotic stenosis, but the roux-en-Y jejunostomy technique of TED makes it unlikely.
Barrett esophagus is rare in children without GERD (prevalence 0.12% (11)), whereas gastric metaplasia arises in approximately 15% of patients with EA (12). Because our 3 patients had severe GERD before TED, gastric metaplasia may already have been present at the time of TED and developed secondarily; however, none of them had a macroscopic aspect suggesting Barrett esophagus on the upper gastrointestinal endoscopy procedures performed before TED. Another hypothesis is that at the time of TED a small remnant gastric mucosa was conserved and grew later on. This is unlikely because only 1 patient had cardial-type Barrett esophagus. Whatever the underlying causes of gastric metaplasia, 1 important point is that we did not find intestinal metaplasia or dysplasia in our patients.
Our results warrant a long-term follow-up into adulthood for every patient with EA undergoing TED. Because symptoms are mild, nonspecific, or even absent, the decision for endoscopy cannot be based only on symptomatology (13–15). Patients with gastric metaplasia are at high risk for later development of dysplasia and cancer and would benefit from a lifelong endoscopic surveillance (16). Our study shows that Barrett esophagus and esophagojejunal anastomotic stenosis should be added to the long list of causes of feeding disorders in patients with TED. These 2 new long-term complications emphasize the need for a case-by-case careful discussion of TED that should be avoided in patients with EA.
1. Holschneider P, Dübbers M, Engelskirchen R, et al. Results of the operative treatment of gastroesophageal reflux in childhood with particular focus on patients with esophageal atresia. Eur J Pediatr Surg
2. Bianchi A. Total esophagogastric dissociation: an alternative approach. J Pediatr Surg
3. de Lagausie P, Bonnard A, Schultz A, et al. Reflux in esophageal atresia, tracheoesophageal cleft, and esophagocoloplasty: Bianchi's procedure as an alternative approach. J Pediatr Surg
4. Lall A, Morabito A, Bianchi A. “Total gastric dissociation (TGD)” in difficult clinical situations. Eur J Pediatr Surg
5. Dipaola G, Camoglio FS, Giacomello L, et al. Complicated total esophagogastric dissociation: case report. Pediatr Med Chir
6. Morabito A, Lall A, Lo Piccolo R, et al. Total esophagogastric dissociation: 10 years’ review. J Pediatr Surg
7. Madre C, Serhal L, Michaud L, et al. Prolonged enteral feeding is often required to avoid long-term nutritional and metabolic complications after esophagogastric dissociation. J Pediatr Gastroenterol Nutr
8. Zaidi T, Sudall C, Kauffmann L, et al. Physical outcome and quality of life after total esophagogastric dissociation in children with severe neurodisability and gastroesophageal reflux, from the caregiver's perspective. J Pediatr Surg
9. Legrand C, Michaud L, Salleron J, et al. Long-term outcome of children with oesophageal atresia type III. Arch Dis Child
10. Dutta HK, Mathur M, Bhatnagar V. A histopathological study of esophageal atresia and tracheoesophageal fistula. J Pediatr Surg
11. Nguyen DM, El-Serag HB, Shub M, et al. Barrett's esophagus in children and adolescents without neurodevelopmental or tracheoesophageal abnormalities: a prospective study. Gastrointest Endosc
12. Jeurnink SM, van Herwaarden-Lindeboom MY, Siersema PD, et al. Barrett's esophagus in children: does it need more attention? Dig Liver Dis
13. Lindahl H, Rintala R, Sariola H. Chronic esophagitis and gastric metaplasia are frequent late complications of esophageal atresia. J Pediatr Surg
14. El-Serag HB, Gilger MA, Shub MD, et al. The prevalence of suspected Barrett's esophagus in children and adolescents: a multicenter endoscopic study. Gastrointest Endosc
15. Castilloux J, Bouron-Dal Soglio D, Faure C. Endoscopic assessment of children with esophageal atresia: lack of relationship of esophagitis and esophageal metaplasia to symptomatology. Can J Gastroenterol
16. Schneider A, Michaud L, Gottrand F. Esophagal atresia: metaplasia, Barrett. Dis Esophagus