Esophageal replacement is indicated when the native esophagus fails to serve as a conduit between the pharynx and stomach. In the pediatric population, the main indications include esophageal atresia and stricture secondary to gastroesophageal reflux or the ingestion of corrosive agents. Tissues derived from the colon, stomach, and jejunum have been used to replace the esophagus, but colon interposition is the most popular surgical option.
Regardless of the technique employed, complications associated with esophageal replacement are frequently observed. Early complications, occurring within the first year following surgery, have been well described (1–10). Late complications (occurring >1 year after surgery) rarely have been evaluated, even more rarely for cases in which intervention was performed in childhood, and information is scarce on the functional outcome in adulthood of such surgery performed during childhood (1–10). The aim of the present study was to evaluate the long-term nutritional, digestive, and respiratory outcome of children undergoing colon interposition for esophageal replacement.
PATIENTS AND METHODS
The medical records of 32 children who underwent colon interposition for esophageal replacement at the Jeanne de Flandre Children's Hospital in Lille, France, between 1970 and 2001 and who remained alive at least 1 year after surgery were reviewed. Table 1 provides demographic data and the indication for esophageal replacement. Informed consent was obtained for all of the patients participating in the study.
Complications were defined as events related to the colon interposition that were life-threatening or required inpatient hospitalization or prolongation of existing hospitalization; that resulted in significant symptoms, disability, or incapacity; or that required adjunct medication or discontinuation of medication. Complications were defined as early when occurring within the first month after operation and late when occurring more than 1 month and less than 1 year postoperatively. Long-term complications were defined as occurring more than 1 year postoperatively. We limited our report to complications strictly related to the colon interposition. We were able to assess early complications in all 32 patients. Twenty-eight patients were able to participate in the cross-sectional aspect of this study.
Patients completed a 24-hour food diary and a questionnaire that assessed age, weight, height, and respiratory and digestive symptoms. This questionnaire did not include any specific quality-of-life questions, but open questions were posed to the parents to gain a subjective view about their child's health and well-being.
All of the patients received a clinical evaluation during which pubertal status and digestive, respiratory, and orthopedic problems were recorded. Anthropometric data were converted into z scores of weight to height (W/H), weight to age (W/A), and height to age (H/A) with reference to the French growth charts of Sempé (11). Lung function tests also were performed. For children younger than 7 years, airway resistance was measured by the interrupter technique (Spirodyn'R, Dyn'R, Muret, France) and the functional residual capacity was measured by the helium dilution method (Medisoft, Sorinnes, Dinant, Belgium). For older patients, plethysmography was used (MasterScreen Body, Jaeger, Hoechberg, Germany): pulmonary volume (functional residual capacity, total lung capacity [TLC], residual volume, current volume) and peak flow (maximum expiratory volume exhaled in 1 second [FEV1]) were measured according to European Respiratory Society/American Thoracic Society standards (12). Obstruction (FEV1/current volume) and distension (residual volume/TLC and functional residual capacity/TLC) were then estimated. All of the variables were expressed as a percentage of normal values. Data obtained from the food diaries were analyzed using Bilnut 3 software (Nutrisoft, Cerelles, France).
Variables were compared using the Student t test. Qualitative parameters were compared using the Fisher exact test. Analysis of variance was used to assess evolution of the anthropometric parameters. Significance was set as P < 0.05.
Data about early complications were available for all 32 patients, and of those 20 were able to complete questionnaires assessing long-term complications. Twelve patients also agreed to undergo respiratory investigations. Minimal follow-up was 14 months; maximal follow-up was 20 years, 9 months. Follow-up was longer than 5 years for 25 subjects (1 patient died 14 months after surgery, and 3 patients were lost to follow-up at 1.2, 1.5, and 4.5 years postoperatively). Follow-up was longer than 10 years for 15 subjects.
Early complications during the first month postoperatively occurred in 17/32 patients (53%) and are reported in Table 2. Late complications occurring during the first year were observed in 5 of 32 patients (15%), all of whom had esophageal atresia (4 cases of cologastric reflux, 1 of portal hypertension). Notably, no complications were observed during the first postoperative year in children who had caustic esophageal stenosis (P < 0.05). There were no deaths.
Long-term complications were observed in 27 of 32 patients (84%) and are reported in Table 3. They tended to be more frequent in esophageal atresia (12/17) than in the ingestion of corrosive agents (5/15), but this did not reach significance. The 4 most frequent complications (stricture, bezoars, graft redundancy, and anemia) were observed during the first 5 years of follow-up. Other complications were observed throughout the follow-up.
It was possible to analyze 9 of 12 patients who completed the 24-hour self-administered food record. Median dietary intake was 106% of the recommended daily allowance (range 84%–196%).
At the endpoint of this study (median age 14 years, 3 months, range 1.5–25 years), 8 of 32 patients (25%) had a W/A z score of less than −2 standard deviations (SD), 4 of 32 (12%) had a W/H z score of less than −2 SD, and 6 of 32 (18%) had an H/A z score of less than −2 SD. Six children with esophageal atresia (35%) and 2 who had ingested corrosive agents (13%) had a W/A z score and/or W/H z score of less than −2 SD (not significant). Five children with esophageal atresia (30%) and 1 who had ingested corrosive agents (6%) had a H/A z score of less than −2 SD (not significant). Where the z scores of W/H, W/A, and H/A were found to be less than −2 SD, they were not associated with respiratory complications. During follow-up, there was no significant evolution of the nutritional status over time as evaluated by analysis of variance.
Although 18 patients had reached puberty by the end of the study, 4 of 18 (22%) had delayed puberty (lack of development of sexual maturation above 11 years for girls and 13 years for boys).
Of the patients, 11/32 (34%) had scoliosis (7 of whom had undergone a thoracotomy) and 2/32 (6%) had kyphosis. At the final evaluation, accurate symptomatic assessment was possible in 20 of 28 patients. Of these 20, 17 had digestive symptoms including abdominal pain (60%), dysphagia (50%), prolonged time taken to eat (50%), coughing while eating (40%), diarrhea (40%), substernal postprandial heartburn (35%), halitosis (20%), and regurgitating and vomiting (20%). Five (25%) received treatment for digestive symptoms (2 antisecretory, 2 antispasmodics, and 1 antacid). Ten patients (50%) had respiratory diseases (asthma, recurrent pneumonia, and recurrent bronchitis) and 13 of 20 (65%) had chronic otorhinolaryngological problems. Of the parents asked for a subjective evaluation of their child's well-being, 17 of 20 responded positively, expressing that they believed that their child was well.
Lung function tests were performed in 12 patients. Of these, 6 (50%) had restrictive lung disease (TLC <20% of normal values), 5 had a spinal deformity, and 2 had respiratory insufficiencies (hypoxemia ± hypercapnia). Two of the 12 patients (16%) had obstructive lung disease (FEV1 <88% of normal values and FEV1/current volume <0.7) and 5 (42%) had normal respiratory function. There was no significant association between restrictive lung disease and the indication for colon interposition (5/8 esophageal atresia vs 1/4 ingestion of corrosive agents). Respiratory complications were not significantly associated with digestive symptoms (5/18 children presenting with digestive symptoms vs 2/14 children presenting without).
Our study demonstrated a high rate of complications and poor long-term functional outcomes after colon interposition, given that more than 50% of the population presented with late complications (<1 year postoperatively) and 80% with long-term complications (>1 year postoperatively). Because we observed that the rate of complications increased with the duration of follow-up (ie, pubertal delay, scoliosis), and have a follow-up of >10 years for only 15 of our patients, the overall rate could be higher than we observed here.
As has been reported in numerous previous studies, we found that the most common early and late complications of colon interposition in children include anastomotic leakage, fistulae, and pulmonary complications (pneumonia, pneumothorax, and aspiration). Death is now rare, and most postoperative complications occurred within the first few weeks and were corrected within the few months following surgery (1–10). With regards to long-term complications, it was found that graft redundancy, cologastric reflux, anastomotic stricture, intestinal obstruction due to adhesions, graft necrosis, cosmetic deformity of the thorax, and respiratory complications are not infrequent (1–10). Furthermore, we found that long-term complications were frequent: more than 80% of children presented with digestive symptoms, the most frequent of which (stricture, bezoars, graft redundancy, and anemia) were observed during the first 5 years of follow-up. Other common complications included respiratory and nutritional symptoms: 25% of patients presented with either an abnormal respiratory function or undernutrition and/or delayed puberty (probably due to undernutrition), and more than 30% had scoliosis.
Aspiration-induced respiratory infections occurring in the postoperative period have been well documented and are frequently associated with asthma (2,3,13). Fifty percent of participants in this study presented with chronic pulmonary manifestations at long-term follow-up. Previous research has shown that recurrent infections are probably due to cologastric reflux from stomach and airway hyperreactivity. Wheezing is relatively common in patients with repaired esophageal atresia, regardless of the technique used, and may be due to events in early childhood such as chronic aspiration rather than to atopy (13). Previous studies assessing pulmonary function after the treatment of esophageal atresia showed that obstructive defects are present in 12% to 54% of patients, restrictive defects in 20% to 49%, normal lung function in 23% to 48%, and mixed restrictive–obstructive defects in 0% to 11% (3,13). Our results at follow-up produced similar figures, suggesting that these pulmonary alterations may well persist long term.
At the endpoint of our study, nearly one third of the study population could be considered to be suffering from moderate undernutrition, yet daily energy intake was adequate, if not exceeding recommended daily allowances. Thus, these data suggest that patients with esophageal replacement may require increased energy intake. However, malabsorption due to colonic bacterial overgrowth, diarrhea, and vomiting or increased energy expenditure due to chronic respiratory disease—which were frequently observed in our population—could also contribute to undernutrition. As in most studies, no improvements in nutritional status were observed in our patient population over time, suggesting that in addition to undernutrition originating in early life (prematurity, socioeconomic status, and feeding difficulties due to esophageal obstruction), energy intake after surgery was insufficient to cover both baseline nutritional requirements and to reverse a state of undernutrition (4,7–9).
Successful functional outcome of esophageal replacement usually is assessed by the ability to swallow a normal diet. In our population, only 1 patient presented with persistent swallowing difficulties, and most parents considered their child to be well and unperturbed by transient, minor symptoms. Nonetheless, consistent with the results of previous studies, nearly 50% of patients had persistent feeding difficulties such as excessive time required for meals, regurgitation, substernal postprandial heartburn, and abdominal pain, sometimes requiring treatment (1,2,4,5,7,9,10,14,15). Perhaps the evaluation of quality of life by the children themselves would yield rather different, possibly worse, reports of their subjective experience when compared with parental views. Quality of life should be considered as a highly relevant endpoint in the evaluation of long-term outcomes of such patients. Further well-designed studies with this particular endpoint in mind need to be carried out.
Chest wall deformities are common in individuals with a history of esophageal atresia and can be due to previous surgery or to vertebral anomalies. Thus, it is not surprising that vertebral deformations, such as scoliosis and occasionally kyphosis, were observed in one third of our patients (16).
No routine endoscopic surveys were carried out in our patients. However, several observations in populations such as this—including a risk of chronic bleeding due to ulceration, metaplasia, and even carcinoma—have subsequently emphasized the importance of endoscopy in long-term follow-up (2,7–9,14,17–21).
Strategies recently have been developed in an attempt to improve the long-term outcome in patients with a nonfunctional esophagus. Tissues from the stomach, ileum, and jejunum have been used as alternatives to colon interposition, but these also have demonstrated a high prevalence of both early and late complications (6,9,22–24). Most physicians and surgeons agree that the native esophagus serves as the best conduit and should be salvaged whenever possible. Where long-gap esophageal atresia is concerned, some authors propose esophageal or stomach elongation (25–29). In the case of caustic injuries, medical alternatives such as endoscopically guided steroid injections, stenting, or local application of mitomycin C could help contribute to the avoidance of esophageal replacement (30–32). Early outcomes of such techniques seem to be rather promising, but long-term results are still scarce (27,29,32).
We would like to thank Chivon Winsloe from the medical faculties of Cambridge University and King's College, London, UK, for help with translating and editing.
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