What Is Known
- Growth and feeding problems have been described in children with esophageal atresia.
- There are many associated gastrointestinal and respiratory complications in patients with esophageal atresia, which may contribute to this.
What Is New
- Infants, children with history of prior fundoplication, those at risk of aspiration and children who have multiple surgeries in the first year of life are associated with malnourishment.
- Early intervention from a dietitian and speech pathologist in the context of a multidisciplinary clinic may be beneficial to support adequate weight gain and grading up to family foods.
Esophageal atresia (EA) is a congenital anomaly of the esophagus with an incidence of approximately 1 in 2500 to 1 in 4500 live births (1,2). With improvements in surgical care resulting in survival rates exceeding 90%, the ongoing and long-term morbidity of these patients has been brought into focus (3). The morbidity in this cohort has many possible etiologies, which may be due to the presence of an associated syndrome in addition to gastrointestinal and respiratory complications. Commonly these include gastroesophageal reflux disease (GERD), esophageal dysmotility, esophageal strictures, pulmonary aspiration, respiratory infections, and tracheomalacia (4–6). Eosinophilic esophagitis (EoE) has also more recently been described in patients with EA with the incidence higher than in the general population (7). These associated complications may have an effect on the feeding development, nutrition, and growth in children with EA. The barriers to optimal oral intake and growth in children with EA are an important concern to clinicians and families and a particular focus of emerging specialist multidisciplinary EA clinics.
Although there is no universal definition of a feeding problem, red flags for identifying feeding difficulties have been described. These include lengthy mealtimes; coughing, choking, and vomiting during meals; oral aversion or food refusal resulting in extreme selectivity; and parental reports of difficult or stressful mealtimes (8). Puntis et al (9) first identified feeding difficulties in children with EA with lengthy mealtimes, choking or coughing during eating, and food refusal the predominantly reported issues. These difficulties were more common in the first 2 years of life compared with a control group of healthy children.
Feeding difficulties can initially develop as a result of medical complications, but over time ongoing feeding difficulties may be maintained by behavioral factors (10,11). Ongoing aversive events in children with EA such as vomiting, coughing, choking, and food impaction can delay feeding skills and reduce their interest in feeding (9,12). A period of tube/gastrostomy feeding is required early on in children with EA and delayed primary repair, especially in the long gap EA cohort (13). Mason et al (14) highlighted the effect of tube feeding can have in progressing to oral feeding during infancy due to reduced experience and adverse effects such as vomiting. The authors highlighted the need to identify contributing factors affecting successful transitioning to oral feeding, including exposure to taste and textures during sensitive periods, such as the first year of life (14).
Poor growth has been shown to be an issue for some children with EA, particularly in the first few years of life (6,9,15). Reduced oral intake is likely to be attributable to many factors discussed above including GERD, dysphagia, and esophageal strictures. Ramsay and Birnbaum (12) highlighted the need for a multidisciplinary team approach in managing patients with EA, due to the significant morbidity in this population and the effect on maternal well-being. A multidisciplinary EA clinic was established at the Sydney Children's Hospital, Randwick (SCHR) in 2011. The EA clinic includes clinicians from general surgery; ear, nose, and throat surgery; gastroenterology; respiratory; dietetics; speech pathology; and social work and has a nurse clinic coordinator.
The primary aim of the present study was to provide a cross-sectional snapshot of nutrition, growth, and problematic mealtime behaviors within the EA population at SCHR at initiation of the multidisciplinary clinic. A secondary aim was to investigate factors associated with poor growth and problematic mealtime behaviors in this cohort.
The present study was a retrospective audit of all children referred to the SCHR multidisciplinary EA clinic during 2011 to 2014. The children had undergone their initial surgical repair at SCHR between 1994 and 2013. Children were most commonly referred to the EA clinic by their managing surgeon, pediatrician, or local medical practitioner for multidisciplinary long-term follow-up. Specific medical reasons that prompted the referral were a choking episode, or further investigation in to their dysphagia or reflux. Patients who had their initial repair at SCHR but had not been referred to the EA clinic were excluded as sufficient data could not be obtained.
Demographic, medical, nutrition, and mealtime behavior data were collected from their first clinic appointment. Specific data collected included age, gestational age, sex, type of EA, primary versus delayed anastomosis, presence of long gap EA, and associated syndromes. Associated gastrointestinal and respiratory complications including fundoplication, tracheomalacia, EoE, GERD, dysphagia, aspiration risk, strictures requiring dilatations, and chest infections were also documented.
Definitions are available online as Supplemental Digital Content (http://links.lww.com/MPG/A819).
Weight, length/height, and weight for length/body mass index (BMI) were plotted on Centers for Disease Control and Prevention 2000 growth charts for each child, z scores were obtained, and growth data of children born prematurely (<37 weeks) were corrected for gestational age until 2 years of age. Children were classified as wasted if their weight for age z score was <−2 standard deviations (SDs), malnourished if their weight for length/BMI z score was <−2 SD, and stunted if their length/height for age z score was <−2 SD (16,17).
The presence of problematic mealtime behaviors was determined based on the entry in the clinic notes by the dietitian and/or speech pathologist. Problematic mealtime behaviors were categorized as not accepting age/developmentally appropriate textures, lengthy mealtimes, extreme food selectivity, and challenging meal times. These categories were chosen because the dietitian and speech pathologist have found these to be common issues in children with EA. Lengthy mealtimes were defined as >45 minutes on a regular basis, irrespective of age. This time period was chosen as mealtimes consistently taking >30 minutes have been shown to be a red flag for feeding problems (8). Extreme food selectivity was defined as having <20 foods in their diet to distinguish between typical picky eating that is commonly reported in young children (18). Challenging mealtimes were defined as regular food refusal events resulting in stressful mealtimes and was based on parental report (8).
Parametric variables were compared with a 2-tailed t test and presented as mean ± SD unless stated otherwise. Categorical variables were compared by 2 tailed Fisher exact test or Chi square with data presented as number (percentage). Statistical significance was accepted if the P value is <0.05. Statistical analysis was performed using Graph Pad 5 for Windows (Graph Pad Software Inc., San Diego, CA).
The study was approved by the Sydney Children's Hospitals Network Human Research and Ethics Committee.
Seventy-five children attended the SCHR multidisciplinary EA clinic between 2011 and 2014 (30 boys and 45 girls). Table 1 documents the patient demographics at the time of their initial appointment. The median age at initial appointment was 3.7 years (range: 0–16.8 years). The majority of children (71%) had type C EA. Five (7%) had type A, 10 (13%) had type B, 1 (1%) had type D and 1 (1%) had type H, and 3 (4%) were not able to be classified from their records. Thirty children (40%) were born premature. Twenty-one (28%) children had an associated syndrome: 12 with VACTERL, 4 with VATER, 3 with Horner syndrome, 1 with Poland syndrome, and 1 with CHARGE. One child had severe scoliosis. Thirty-four patients (45%) had at least 1 surgery in their first year of life in addition to EA repair, including fundoplication, insertion of gastrostomy, aortopexy, cardiac surgery, and anorectal surgery.
Gastrointestinal and Respiratory Complications
The incidence of gastrointestinal and respiratory complications in the cohort is presented in Table 1. Seventy-two children (96%) had at least 1 associated gastrointestinal or respiratory complication. Of the 65 children (87%) who were described as having GERD, 42 were diagnosed via endoscopy and biopsy/pH-impedance testing and 23 were based on symptom questionnaire. Indications for investigations were due to symptoms such as vomiting, gagging, heartburn, or coughing with feeds. Eighteen fundoplications were performed in this cohort, with the procedure performed at a median age of 10 months of age (range 3 months to 3 years 4 months). Nineteen out of 50 children (38%) who had had an endoscopy or biopsy were shown to have EoE.
Twenty-four children (32%) had a history of gastrostomy feeding. Ten children were still using their gastrostomy at their initial EA clinic appointment (median age 15 months, range 5 months to 6 years). Two of these children were receiving gastrojejunal feeds. One child was “nil by mouth” due to risk of direct aspiration and severe reflux and the remainder had supplementary tube feeds due to oral aversion. Three children with a gastrostomy also had a fundoplication for severe reflux. Five children (7%) were receiving oral nutrition support at the time of their initial clinic appointment.
At the initial clinic appointment, 13 (18%) children were wasted, 7 (9%) were malnourished, and 7 (9%) were stunted (Table 2). The weight for length/BMI z scores ranged from 2.33 to –4. 27, with a mean of –0.4 (±1.2). Two children (3%) had a weight for length/BMI z score <–3 SD, indicating severe malnutrition (16). Two children (3%) were overweight (weight for length/BMI z score >2).
Association Between Demographic/Gastrointestinal and Respiratory Complications and Growth
Infants had significantly poorer growth, compared with children older than 1 year (P < 0.05) (Fig. 1A) as did those who had undergone fundoplication (P < 0.05) (Fig. 1B) were at risk of direct aspiration (P < 0.05) (Fig. 1C) or those children who had surgery in the first year of life apart from EA repair (P < 0.05) (Fig. 1D). No other demographic or gastrointestinal/respiratory complications were significantly associated with poor growth (Table 3).
Fifty-six children (75%) were reviewed by the dietitian and/or speech pathologist at their initial appointment in the EA clinic and were analyzed for problematic mealtime behaviors. The reasons for the other children not being seen were the dietitian or speech pathologist not being present on the day, or due to time constraints in clinic. The 19 children who were not assessed by the dietitian and/or speech pathologist were excluded from mealtime behaviors analysis. Forty-four children (79%) had at least 1 problematic mealtime behavior with 30 (54%) children not consuming age/developmentally appropriate textures, 16 (29%) demonstrating extreme food selectivity, 16 (29%) had challenging mealtime behaviors, and 14 (25%) had lengthy mealtimes.
Of the 30 children not consuming age/developmentally appropriate textures, the reasons attributed were parental perceived difficulty with oro-motor skills or concern about risk of food impaction/choking (n = 12), underlying medical cause such as EoE, recent respiratory illness or aspiration risk (n = 6), medical advice following recent history of food impaction, or prior fundoplication (n = 4). For the remainder of children (n = 8) the reason was not reported in the notes or they had an unspecified feeding difficulty. All of the children who were still using their gastrostomy were not accepting age-appropriate textures and had extreme food selectivity, highlighting the importance for ongoing dietetic and speech pathology evaluation and consultation after gastrostomy placement.
Younger children were less likely to be eating age-appropriate textures (P < 0.05) (Fig. 2A). Seventy-two percent of children aged 0 to 2 years were not eating age-appropriate textures, which reduced to 65% for children ages 2 to 5 years and 30% in children older than 5 years. There was no significant association between age and time taken to complete meals, presence of challenging mealtime behaviors, or extreme food selectivity (Fig. 2B–D). There was no significant association between the presence of problematic mealtime behaviors and growth or demographic or gastrointestinal and respiratory complications.
The present study demonstrates the prevalence of nutritional impairment and challenging mealtime behaviors in children with EA. The majority of our cohort analyzed were not consuming age-appropriate textures, particularly younger children. In addition, the present study highlights the important association between infants with EA and malnourishment.
The present study demonstrates that in the cohort of children with EA attending a multidisciplinary clinic, infants were more likely to have worse growth compared with older children at initial appointment. In the study by Seo et al (19) of 97 infants with EA, 48% had weight less than the 10th percentile at 1 year and 40% at 2 years. The majority of surgical procedures and prolonged hospitalization in patients with EA occurs within the first year of life (20), which could explain why lower weight for height z scores commonly occur in infancy. As surgical procedures in the first year of life were associated with worse growth, this highlights the need for early intervention in these patients. Legrand et al (21) reported 9% of patients were undernourished using weight for height z scores. Poor growth in patients with EA has previously been shown to improve with age (6,22). In the study by Lacher et al (22), 70% of patients had a weight less than the 25th percentile at 1 year of age, which reduced to 41% by 10 years of age. Similarly, Little et al (6) showed weight and height improving with age, with the amount of children with weight less than the 25th percentile reducing from 49% at 5 years to 31% at 10 years.
In the current cohort, children who had prior fundoplication were more likely to have worse growth. In individuals with EA, esophageal dysmotility is almost universal. The need for fundoplication in a select group of patients implies severe GERD, with likely repeated aspiration and/or recurrent pneumonia and may make this dysmotility even worse (23).
Children at risk of direct aspiration were also more likely to have worse growth. Feeding difficulty due to poorly coordinated swallow, increased risk for chest infections and hospitalizations could all possibly contribute to risk of aspiration. Mahoney and Rosen (24) highlighted that aspiration can be a cause of respiratory symptoms and feeding difficulties. The lack of significant association between other gastrointestinal and respiratory complications with worse growth in the present study may be due to the retrospective nature, which limited complete data collection and small sample size.
Interestingly the presence of problematic mealtime behaviors was not associated with poor growth. This may be due to the fact that all of the children who were determined to have extreme food selectivity or challenging mealtime behaviors had a gastrostomy in use at initial appointment. Similarly there was no association between problematic mealtime behaviors and demographic or gastrointestinal/respiratory complications.
One of the major finding of our study was that more than half of the current cohort analyzed for problematic mealtime behaviors were not eating age-appropriate textures, particularly younger children. The ability to manage textured food in typically developing healthy children becomes more efficient with age (25). Choking, dysphagia, GERD, and respiratory infections may limit the exposure to and/or acceptance of textured foods in the early years in the EA cohort, through child avoidance, medical advice, or parental reluctance. Although the concept of a critical period for accepting textured food is often cited (26), providing a wide range of tastes that is acceptable to children not managing age appropriate textures may promote a more positive mealtime experience. Parents require support in progressing with textured food.
There are several limitations to the present study. Because of the retrospective nature of the present study not all data were available for all patients in the study cohort. Twenty-five percent of the cohort was not assessed by a dietitian/speech pathologist, which could have altered the results, because children with feeding problems may have been more likely to be seen. Selection bias is another limitation because not all patients who had an EA repair at SCHR over the time period studied were included in the review. We had a lower proportion than the general proportion of type C EA. Potentially the more motivated parents may have attended our clinic or doctor referrals may have been arranged for the more complex children. Furthermore parental report of feeding difficulties is highly subjective. Because this was a retrospective study, validated feeding assessment questionnaires were not used. This limits the ability for direct comparison with other studies. Future studies in this population should include validated feeding assessment questionnaires, such as the Montreal Children's Hospital Feeding Scale (27), to help identify problematic mealtime behaviors. The use of dysphagia scores is also recommended to define the true incidence of dysphagia in the cohort.
A further limitation is that there is no universal definition for malnutrition in children. BMI z scores were chosen as this measurement was available in a retrospective audit for patients ages up to 16 years. The authors acknowledge that this does not take in to account body composition and is not the most sensitive measure to assess growth in children. Future studies should look at the association between stunting (height for age z scores) and gastrointestinal/respiratory complications. Because of the incidence of stunting, mid parental height should also be used in future studies to determine target height. Finally, creating standardized terminology for problematic mealtime behaviors and malnutrition within the EA population would be useful for identifying and monitoring progress in this at risk population and allow for comparison of results across centers.
Despite these limitations this is one of the few studies in the literature, which evaluates malnutrition and problematic mealtime behaviors in children with EA. Furthermore this is one of the largest to assess children with EA attending a multidisciplinary clinic. In the present study we found that younger children with EA were particularly at risk of poorer nutrition, which highlights the importance of early intervention in this cohort. Our study emphasizes the significant presence of gastrointestinal and respiratory complications within this cohort and highlights the need for follow-up by a specialist multidisciplinary team for all children with EA. Long-term prospective studies should be conducted using a validated feeding assessment questionnaire and dysphagia scores to determine risk factors for growth and feeding problems in these patients and to monitor improvements over time.
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Supplemental Digital Content
© 2017 by European Society for Pediatric Gastroenterology, Hepatology, and Nutrition and North American Society for Pediatric Gastroenterology,