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school support in children with repaired esophageal atresia
Journal of Pediatric Surgery 53 (2018) 1970–1975
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Clinical predictors and prevalence of receiving special preschool/school support in children with repaired esophageal atresia Michaela Dellenmark-Blom a,⁎, Linus Jönsson b, Vladimir Gatzinsky b, Kate Abrahamsson a,b a b
Department of Pediatric Surgery, Queen Silvia Children's Hospital, Sahlgrenska University Hospital, 416 85 Gothenburg, Sweden Institute of Clinical Sciences, Department of Pediatrics, Gothenburg University, The Queen Silvia Children's Hospital, 416 86 Gothenburg, Sweden
a r t i c l e
i n f o
Article history: Received 11 September 2017 Received in revised form 21 November 2017 Accepted 22 November 2017 Key words: Esophageal atresia Tracheoesophageal fistula Psychosocial functioning School support Educational support Feeding difficulties
a b s t r a c t Background/purpose: In a sparsely investigated field, we aimed to evaluate the use of special preschool/school support among children with repaired esophageal atresia (EA) and/or tracheoesophageal fistula (TEF), the predicting clinical factors for this support, and level of school absence. Methods: Data on 119 EA/TEF children 2–17 years old were collected through medical records and questionnaires (response rate 95%). Logistical regression analysis identified clinical predictors of special preschool/school support in the population without genetic disorders (n = 105). Nominal hypothesis testing was performed using Fisher's exact test (p b 0.05). Results: Of the 119 children, 35.3% received special preschool/school support; 26.8% educational support, 21.8% support with nutritional intake issues and 13.4% received both types of support. Educational support was independently predicted by birth weight b 2500 g (p = 0.026) and associated anomalies (p = 0.049), nutritional intake support by gastrostomy insertion (p = 0.0028), and both types of supports by major revisional surgery (p = 0.0081). School absence ≥1 month/year, present in 25.5% of the children, was more frequently reported in children receiving preschool/school support, in preschoolers and in those with persistent respiratory problems (p b 0.05). Conclusions: Special preschool/school support is provided for approximately one-third of EA/TEF children. In EA/ TEF children without genetic disorders, use of this support is predicted by congenital and surgical factors, and related to frequent school absence. © 2017 Elsevier Inc. All rights reserved.
Following surgical repair of esophageal atresia (EA) and/or tracheoesophageal fistula (TEF), survival rates now exceed 90% [1], but late morbidity is significant. Dysphagia, gastroesophageal reflux disease [2,3], feeding difficulties [4] and respiratory problems [5,6] such as wheezing, chronic cough, and repeated airway infections may affect children with EA/TEF. Little is, however, known about the psychosocial outcomes. EA/TEF children are reported having both comparable [7] and lower intelligence [8,9] levels than healthy children. Different studies have shown both psychosocial functioning in EA/TEF children to be similar [10] to the general population, but also worse [7–9]. In a literature review from 2016, IJsselstijn et al. [11] concluded that EA/TEF children are at risk of developing school problems. However, this field is
⁎ Corresponding author at: Department of Pediatric Surgery and Urology, The Queen Silvia Children's Hospital, 416 85, Gothenburg, Sweden. Tel.: +46 313434372; fax: +46 31843453. E-mail addresses: [email protected] (M. Dellenmark-Blom), [email protected] (L. Jönsson), [email protected] (V. Gatzinsky), [email protected] (K. Abrahamsson). https://doi.org/10.1016/j.jpedsurg.2017.11.057 0022-3468/© 2017 Elsevier Inc. All rights reserved.
sparsely investigated. In one study [8], 22% of EA/TEF children were in special education (sample ntot = 36, age 8–12 years old) and in another study [10], 33% (sample ntot = 21, age 12–17 years old) of the subjects. In a third study, 10% of children with the condition (sample ntot = 60, primary school-age) attended school for mentally handicapped children [12]. EA/TEF children with associated anomalies, which are present in around 55% [1] of the group, are almost three times more likely to require special education [13], and function more poorly at school, particularly if they have cardiovascular anomalies [14]. Children born with imperforate anus and multiple anomalies (which could include EA), are also more likely to be in special education [13]. To date studies are few [8,10,13,14], include mostly small samples, exclude children of preschool age, and do not properly explain the relationship between clinical factors and school problems. In Sweden, between 5% and 6% of the pupils in elementary school received special educational interventional support, and 1% attended school for children with learning disabilities [15,16], but investigations aiming to describe the school conditions for EA/TEF children are lacking. In this study, we aimed to determine the clinical predictors and prevalence of receiving special preschool/school
M. Dellenmark-Blom et al. / Journal of Pediatric Surgery 53 (2018) 1970–1975
support among children with EA/TEF, and the level of school absence, in a Swedish population. 1. Material and methods 1.1. Patients The study was approved by the regional ethical committee. Parents of children with EA/TEF (Gross A–E) aged 2–17 years, treated between 1997 and 2014 at the Queen Silvia Children's Hospital, Gothenburg, Sweden, were contacted on the phone by a researcher. They received oral information and a study invitation. 137/145 participants accepted written study information, and returned informed consent. 1.2. Data collection The patients' hospital records were reviewed for clinical data up to the time of the study, which included information on neonatal characteristics, surgical treatment(s), associated anomalies/conditions and bronchoscopy results. 130 (94.9%) responded to a standardized postal questionnaire developed by the authors. The first part consisted of sociodemographic and parent/caregiver information (12 questions), and the second part (20 questions) information on the child's age and health status, including five specific questions about the children's preschool/school situation. In Sweden, children attend preschool and preschool-class up six years of age before entering elementary school (grade 1–9) at seven years of age. Upper secondary school (three years) follows after this. The Swedish school law gives all children in preschool/school the right to special school support if needed, preferably delivered in the child's regular class. There are also special schools for children with learning disabilities [15,17]. Families were asked whether the child with EA/TEF attended preschool/school (yes/no), currently had special school support (yes/no), and how frequently the child had been absent from school the previous year (no school absence, one time/year, 2–5 times/year, 6–11 times/year, one time/month, None time/month). The two last questions were followed by open, explorative questions with instructions to parents to further describe the child's special preschool/school support, and list the causes of school absence. A closing question asked parents whether we had omitted to ask any questions which were important to them, and what they were. 1.3. Statistical analysis Statistical analysis was performed using SPSS 22.0 and SAS 9. software. The analysis included 119 children with school attendance (two adolescents dropped out of school, nine families gave no explanation, but seven of these children were younger than for compulsory elementary school). Parents' open answers were categorized into type of preschool/school support and cause of school absence, for evaluation using descriptive statistics (number,%). A priori, we decided to exclude EA/TEF children with genetic disorders from the hypothesis testing. This regarded children with Charge syndrome (n = 5), Apert syndrome (n = 1), Angelman syndrome (n = 1), trisomy 21 and other chromosomal abnormalities (n = 7), with known associations to cognitive, hearing or visual impairments. In the additional sample (n = 105), using predefined hypothesis, univariable logistical regression analysis was performed to identify clinical predictors of special preschool/school support by calculation of odds ratio (OR), 95% confidence interval (CI). The variables included in the models were Neonatal characteristics; child gender, prematurity (gestational age b 37 weeks), low birth weight (b2500 g); Surgery and anesthesia; primary esophageal repair, gastrostomy insertion, any early postoperative complication (recurrent fistula, anastomotic leakage, sepsis, wound infection, pneumothorax with need of drainage, thrombosis), revisional surgery owing to anastomotic leakage or recurrent fistula, N1 anesthesia prior to first hospital discharge, Associated anomalies; associated anomaly, cardiovascular or
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anorectal anomaly, VACTERL association Follow-up; antireflux surgery, dilatation of EA, dilatations of EA N 10 as a criterion for complicated evolution [18], gastrostomy feeding, bronchoscopy-verified severe tracheomalacia/tracheobronchomalacia (an anteroposterior collapse during coughing and expiration documented as ≥75%, excessive and/ or severe [19]), doctor-diagnosed asthma and child-age group at follow-up. Clinical variables resulting in p b 0.1 in the univariable analysis, were included in the multivariable analysis. The significant level for predictors was p b 0.05. The area under the relative (receiver-) operating characteristics (ROC) curve (AUC) was used to estimate the predictor value. AUC N 0.5 is considered acceptable, and AUC of 1.0 equals perfect test [20]. School absence ≥1/month was classed as considerable. We examined whether this was related to specific parent-listed reasons, preschool/school-age and preschool/school support (Fischer's exact test, p b 0.05). 2. Results 2.1. Study population Patient population characteristics (n = 119) are presented in Table 1. 2.2. Prevalence and type of special preschool/school support Out of 119 EA/TEF children, 42 (35.3%) received special preschool/ school support; 32 (26.8%) children used educational support, 9 (7.6%) of whom attended school for children with learning disabilities, and 26 (21.8%) received nutritional intake support. Sixteen (13.4%) EA/TEF children received both educational and nutritional intake support. Following the definitions of special preschool/school support, the prevalence is reported separately for EA/TEF children with genetic disorders (n = 14) and without genetic disorders (n = 105) in Table 2. 2.3. Clinical predictors of special preschool/school support The calculations of OR and AUC in relation to special preschool/ school support in EA/TEF children without genetic disorders (n = 105) are shown in Table 3. The predicting factors of receiving special educational support in the univariable analysis were low birth weight (p = 0.021), N1 anesthesia before first hospital discharge (p = 0.043), associated anomaly (p = 0.042), gastrostomy feeding at follow-up (= 0.0009) and doctor-diagnosed asthma (p = 0.042). Low birth weight (p = 0.026) and associated anomalies (p = 0.049) independently predicted the use of educational support. The predictors of support with nutritional intake issues at preschool/ school in the univariable analysis were gastrostomy insertion (p = 0.0028), revisional surgery owing to anastomotic leakage or recurrent fistula (p = 0.011), associated anomaly (p = 0.031), anti-reflux surgery (p = 0.013), gastrostomy feeding (p = 0.0004), and preschool-age at follow-up (compared to adolescents, p = 0.015). Gastrostomy insertion independently increased the OR by 5.42 (p = 0.0028). The predictors of receiving educational and nutritional intake issues support at preschool/school were revisional surgery owing to anastomotic leakage or recurrent fistula (p = 0.0081) and gastrostomy feeding at follow-up (p = 0.0006) in the univariable analysis, though revisional surgery was the independent predictor (p = 0.0081). 2.4. Level of school absence Information on school absence is shown in Table 4. In EA/TEF children without genetic disorders, school absence ≥1/month was significantly more commonly reported in pupils receiving educational support (47.4% vs 20.28%, p = 0.020), and nutritional intake support (64.7% vs 17.4%, p b 0.001). It was also more common in preschoolers (42.3% vs 19.5%, p = 0.035), and in children with persistent respiratory
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M. Dellenmark-Blom et al. / Journal of Pediatric Surgery 53 (2018) 1970–1975
Table 1 Presentation of the study sample (119 children and their parents). Frequency (%) Child background information Male Gestational week Birth weight (g) Gross A/B/C/D/E Associated anomalies Cardiovascular Gastrointestinal (excluding anorectum) Anorectal Urogenital Limb Vertebral–skeletal Central nervous system Respiratory Eye Ear VACTERL Genetic disorders Primary anastomosis Gastrostomy insertion Number of anesthesia before first hospital discharge Revisional surgery owing to anastomotic leakage or recurrent fistula Follow-up Child age Antireflux surgery Esophageal dilation Gastrostomy feeding at follow-up Doctor-diagnosed asthma Severe tracheomalacia/tracheobronchomalaciaa
a
Median (Min/Max)
36.5 (3.3) 2560 (715)
37 (28/43) 2600 (970/4110)
2.5 (2.5)
2 (1/14)
10 (5)
9 (2–17)
3.4 (11)
0 (0/90)
42 (7)
42 (26/69)
69 (58)
12 (10.1)/6 (5.0)/93 (78.2)/2 (1.7)/6 (5.0) 72 (60.5) 32 (26.9) 9 (7.6) 12 (10.1) 15 (12.6) 9 (7.6) 27 (22.7) 8 (6.8) 4 (3.4) 9 (7.6) 4 (3.4) 19 (16.0) 14 (11.8) 101 (84.9) 43 (36.1) 16 (13.4)
27 (22.7) 49 (41.2) 16 (13.4) 39 (32.8) 18 (15.1)
Parent-report Mother Parental age (years) Highest education university/college Living with cohabitant partner
Mean(SD)
106 (89.1) 59 (49.6) 98 (82.4)
An anteroposterior collapse during coughing and expiration documented as ≥75% [reference [19], excessive and/or severe.
problems (42.3% vs 16.9%, p = 0.014). More preschoolers had school absence ≥ 1/month owing to colds, compared to school-age children (78.6% vs 51.9%, p = 0.015).
2.5. Final open question to parents Five families described additional experiences, as shown in Table 5.
3. Discussion In this study, 35.3% of EA/TEF children received special support in preschool/school. Overall, 26.8% of EA/TEF children received educational support, including 7.6% in a school for children with learning disabilities. Even in EA/TEF children without genetic disorders, the prevalence (18.1%) of educational support seemed higher than in the general Swedish population (5%–6% special educational support)
Table 2 Frequency(%) of special preschool/school support in children with esophageal atresia (EA) and/or tracheoesophageal fistula (TEF). Definition of special school support
SPECIAL SCHOOL SUPPORT
Educational support
School for children with learning disabilities
Support with nutritional intake issues Support with educational & nutritional intake issues
• Educational support, including school for children with learning disabilities • Having support with nutritional intake issues at school • Having a special teacher, school assistant, adjusted learning program, environment or help equipment to support concentration, memory and/or learning • A special school for children with learning disabilities, usually owing to cognitive impairments, who don't achieve the general required school achievement specific to age • Having a teacher/school assistant beside the child during meals for observation or help keeping the correct pace, food consistency, portion sizes, prevent/assist choking episodes or for gaining help with gastrostomy feeding • Jointly having any of the mentioned school supports in the columns educational and nutritional intakes issues
EA, esophageal atresia; TEF, tracheoesophageal fistula. a These patients had major associated malformations.
EA/TEF children with genetic disorders (ntot = 14)
Children with EA/TEF without genetic disorders (ntot = 105)
Number (%)
Number (%)
14 (100)
28 (26.7)
13 (92.9)
19 (18.1)
6 (42.9)
3 (2.9)a
9 (64.3)
17 (16.2)
8 (57.1)
8 (7.6)
Table 3 Calculated odds ratio (OR) and area under the relative (receiver-) operating characteristics curve (AUC) of receiving special educational support in children with esophageal atresia and/or tracheoesophageal fistula (without genetic disorders), using bold text to highlight significant p-values (p b 0.05). EDUCATIONAL SUPPORT
SUPPORT WITH NUTRITIONAL INTAKE ISSUES
Univariable analysis OR (95% CI) NEONATAL CHARACTERISTICS Gender girl Prematurity (GAa b 37 weeks) Low birth weight (b2500 g) SURGERY AND ANESTHESIA No primary esophageal repairb
Any early postoperative complication Revisional surgery owing to anastomotic leakage or recurrent fistula N1 anesthesia before first hospital discharge ASSOCIATED ANOMALIES Associated anomaly Cardiovascular anomaly Anorectal malformation VACTERL association FOLLOW-UP Antireflux surgery Dilatation of EA Dilatations of EA N10 Gastrostomy feeding Broncoscopy verified severe tracheomalacia/tracheobronchomalaciab Doctor-diagnosed asthma
0.8 0.69 (10.29–2.26) 1.66 0.33 (0.60–4.61) 3.37 0.021 (1.20–9.47)
0.53 (0.40–0.65) 0.56 (0.43–0.69) 0.65 3.31 (0.52–0.77) (1.15–9.53)
0.73 (0.15–3.55) 2.58 (0.92–7.29) 1.61 (0.58–4.46) 2.71 (0.80–9.15) 3.22 (1.04–9.99)
Univariable analysis
p-value OR (95% CI) 1.01 (0.35–2.90) 1.43 (0.50–4.07) 1.97 (0.69–5.61)
0.98
0.52 (0.44–0.60) 0.61 (0.48–0.74) 0.56 (0.43–0.69) 0.57 (0.47–0.68) 0.64 (0.52–0.76)
1.50 (0.37–6.07) 5.42 (1.79–16.37) 2.14 (0.73–6.30) 4.79 (1.43–16.06) 2.54 (0.80–8.08)
0.57
3.42 0.042 (1.05–11.13) 2.40 0.099 (0.85–6.78) 0 N/A
0.63 3.35 0.049 (0.53–0.74) (1.00–11.20) 0.59 (0.47–0.72) N/A
1.50 (0.43–5.23)
0.53
0.53 (0.43–0.63)
4.26 (1.14–15.87) 0.82 (0.24–2.77) 2.14 (0.51–9.07) 1.78 (0.50–6.30)
1.43 (0.41–5.06) 0.64 (0.20–2.09) 1.02 (0.98–1.06) 12.77 (2.84–57.46) 1.16 (0.29–4.58) 2.87 (1.04–7.93)
0.58
0.53 (0.41–0.66) 0.55 (0.41–0.69) 0.45 (0.32–0.57) 0.64 (0.53–0.75) 0.51 (0.42–0.60) 0.62 (0.50–0.75)
4.38 (1.36–14.03) 2.54 (0.78–8.25) 1.04 (0.99–1.10) 15.45 (3.37–70.77) 3.25 (0.95–11.16) 2.12 (0.74–6.10)
0.55 (0.41–0.68)
1 0.54 (0.18–1.68) 0.07 (0.01–0.60)
0.69 0.073 0.36 0.11 0.043
0.46 0.30 0.0009 0.84 0.042
0.026
Multivariable analysis
p-value AUC (95% CI) OR (95% CI)
0.51 0.20
0.0028 0.17 0.011 0.11
0.031 0.75 0.30 0.37
0.013 0.12 0.13 0.0004 0.061 0.16
Univariable analysis
p-value OR (95% CI)
Multivariable analysis
p-value AUC (95% CI) OR (95% CI)
0.50 (0.37–0.63) 0.54 (0.41–0.68) 0.58 (0.45–0.72)
1.49 (0.35–6.30) 0.90 (0.20–3.99) 1.62 (0.38–6.88)
0.59
0.53 (0.43–0.63) 0.70 5.42 0.0028 (0.57–0.82) (1.79–16.37) 0.59 (0.46–0.73) 0.63 (0.50–0.75) 0.61 (0.48–0.75)
0.92 (0.10–8.13) 4.05 (0.91–18.10) 2.07 (0.44–9.77) 7.82 (1.71–35.80) 6.07 (0.68–54.01)
0.94
0.65 (0.54–0.76) 0.52 (0.40–0.63) 0.54 (0.44–0.64) 0.54 (0.43–0.65)
2.39 0.30 (0.46–12.43) 1.73 0.48 (0.38–7.76) 0 N/A
0.60 (0.43–0.76) 0.56 (0.37–0.74) N/A
0
N/A
N/A
0.65 (0.51–0.79) 0.61 (0.47–0.75) 0.62 (0.48–0.76) 0.66 (0.54–0.78) 0.59 (0.47–0.71) 0.59 (0.46–0.72)
4.17 (0.78–22.38) 0.29 (0.03–2.71) 1.04 (0.99–1.09) 18.40 (3.52–96.05) 4.25 (0.90–20.10) 3.91 (0.88–17.44)
0.096
0.65 (0.43–0.88) 0.63 (0.43–0.83) 0.46 (0.26–0.65) 0.72 (0.54–0.91) 0.63 (0.44–0.81) 0.66 (0.48–0.85)
0.71 (0.59–0.82)
1 1.64 (0.30–9.15) 0.37 (0.03–4.28)
0.89 0.51
0.067 0.36 0.0081 0.11
0.28 0.087 0.0006 0.068 0.074
p-value
0.55 (0.36–0.74) 0.51 (0.33–0.70) 0.56 (0.37–0.75) 0.50 (0.38–0.63) 0.67 (0.48–0.85) 0.59 (0.39–0.79) 0.69 7.82 0.0081 (0.51–0.88) (1.71–35.80) 0.69 (0.52–0.86)
M. Dellenmark-Blom et al. / Journal of Pediatric Surgery 53 (2018) 1970–1975
Gastrostomy insertion
Multivariable analysis
p-value AUC (95% CI) OR (95% CI)
SUPPORT WITH BOTH EDUCATION AND NUTRITIONAL INTAKE ISSUES
Child age group Preschool age (2–6 years old)c Middle school-age (8–12 years old) Adolescence (13–17 years old)
1 1.52 (0.42–5.54) 1.19 (0.30–4.72)
0.52 0.81
0.29 0.015
0.57 0.42
0.64 (0.47–0.82)
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AUC, area under the relative (receiver-) operating characteristics curve; CI, confidence interval; EA, esophageal atresia; GA, gestational age for birth; N/A, not applicable; OR, odds ratio. Event rate in the specific age groups were; Educational support: preschool age (14.8%), middle school age (20.9%), adolescence (17.1%); Nutritional intake support: preschool age (29.6%), middle school age (18.6%), adolescence (2.9%); Both type of supports: preschool age (7.4%), middle school age (11.6%), adolescence (2.9%). a Delayed primary anastomosis/elongation/esophageal replacement. b An anteroposterior collapse during coughing and expiration documented as ≥75%, excessive and/or severe. c Used as reference group for comparison.
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M. Dellenmark-Blom et al. / Journal of Pediatric Surgery 53 (2018) 1970–1975
Table 4 Information on school absence among children with esophageal atresia (EA) and/or tracheoesophageal fistula (TEF).
School absence the previous year No school absence 1 time 2–5 times 6–11 times ≥1/month Reasons for school absence Colds General sickness such as just “feeling ill”/gastroenteritis/headache Persistent troublesome respiratory symptoms Examinations and doctor-visits at the hospital Out-clinic visits with physiotherapists or nurses Stomachache Pneumonia GER-related symptoms causing sleeping disorders
EA/TEF children with genetic disordersa
Children with EA/TEF without genetic disordersb
Frequency (%) 0 1 (7.7) 2 (15.4) 4 (30.8) 6 (46.2)
Frequency (%) 10 (9.8) 6 (5.9) 37 (36.3) 23 (22.5) 26 (25.5)
6 (46.2)
62 (60.8)
4 (30.8)
29 (28.4)
1 (7.7) 10 (76.9) 5 (38.5) 1 (7.7) 0 3 (23.1)
20 (19.6) 16 (15.7) 6 (5.9) 5 (4.9) 4 (3.9) 3 (2.9)
EA, esophageal atresia; GER, gastro-esophageal reflux; TEF, tracheoesophageal fistula. a One missing information because the child started school during the previous year, calculated on the basis of information gained from 13 children. b Three missing information, calculated on the basis of information gained from 102 children.
[15,16], but slightly lower (22–33%) than indicated in previous studies of EA/TEF children [8,10]. However, the definitions of educational school support and the study populations (i.e. preschool, secondary school) may vary. In agreement with the Hamrick et al. study [13] we found an increased use of special educational support in EA/TEF children with associated anomalies. Impaired school-functioning has been found particularly in EA/TEF children with cardiovascular anomalies [14]. In this study, cardiovascular, anorectal anomalies or VACTERL association did not increase the special preschool/school support. One possible explanation is that sample sizes become smaller when investigating the impact of different types of anomalies. The variable N 1 anesthesia before first hospital discharge, did predict educational support in the univariable analysis, but was not an independent predictor. A possible explanation is that this variable might be a proxy for higher level of morbidity in the EA/TEF patient. In our study sample, the most common reasons for several anesthesias were gap measurements, esophageal dilatation, revisional surgery of EA/TEF repair, gastrostomy insertions, antireflux surgery and broncoscopy examinations needed owing to airway disease. Low birth weight independently predicted use of educational support. Low birth weight and prematurity are interrelated and may extend the neonate's need for mechanical ventilation. This, in turn may increase the risk of poorer neurodevelopmental outcomes, and explain such findings. However, in this study, prematurity, postoperative complications or revisional surgery (associated with possible prolonged mechanical ventilation) did not significantly affect the educational support. Low birth weight (controlled for possible relevant confounders) has been associated with lower intelligence in the general population continuing into late adulthood [21]. This, in common with anomalies described in our study, would support a hypothesis of factors related to fetal development and to the malformation. In comparison, normal intelligence has been demonstrated in EA/TEF children without significant associated anomalies [7]. Several surgical variables predicted use of nutritional intake support in EA/TEF children. Gastrostomy insertion may be required for reasons such as “long-gap EA”, revisional surgery, cyanotic spells, severe GER, or associated anomalies. Some of these indications may vary between centers. Additionally to “long-gap EA”, the main indications for
Table 5 Comments added by five families of children with esophageal atresia (EA) and/or tracheoesophageal fistula (TEF) in explorative questions regarding aspects of importance to them. The child experienced school as hard/demanding The child had difficulties Parents (n = 2) of adolescent boys managing the grades Parents (n = 4), three parents of 2–6 year Prolonged school absence affected social integration and/or old children and one parent of a school achievement teenage boy Parents (n = 3) of children Respiratory symptoms caused 2–6 years old prolonged school absence Repeated needs of hospital admissions One parent of a teenage boy caused prolonged school absence Frequent school absence owing to One parent of a preschool girl misunderstanding of vomiting as gastroenteritis by teachers Parents (n = 2) of adolescent boys
EA, esophageal atresia; TEF, tracheoesophageal fistula.
gastrostomy insertion at our center were severe nutrition difficulties, severe GER or severe tracheomalacia, with risk of failure to thrive. Although the majority of gastrostomies are temporary, a prior insertion may imply a more complex clinical course. Feeding difficulties are a known consequence of EA/TEF repair [4], and gastrostomy may inhibit the development of normal eating behavior. This, and the underlying morbidity, can explain why a prior gastrostomy insertion may influence the need for nutritional intake support at preschool/school. Interestingly, revisional surgery for anastomotic leakage or recurrent fistula independently predicted special preschool/school support for both educational and nutritional issues. Although major revisional surgery is regarded as a criterion for severe EA/TEF [18,22,23], the impact on future sequelae is only partly understood. Anastomotic leakage is associated with stricture development [24]. In this study, esophageal dilatation was not a predictor of special preschool/school support. In the Koivusalo et al. study [25], 42 (16%) EA/TEF patients underwent revisional surgery, and in 92% of the survivors, patients eventually resumed full oral intake. This study suggests that major revisional surgery is associated with significant health care needs in EA/TEF children, necessitating support at preschool/school age. The trend toward higher levels of nutritional intake support among preschoolers with EA/TEF could be explained by feeding difficulties having less impact with increased age [4]. However, this is contradicted by another study [26], and from quality-of-life-studies, suggesting that eating issues may affect EA/TEF children across childhood [23,27]. Another explanation is the development of coping strategies with increased age, which help EA/TEF children to independently deal with nutritional intake issues [28]. No study has previously reported on the relationship between special preschool/school support and school absence in EA/TEF children. In EA/TEF children with genetic disorders health care visits seemed to be the primary cause of school absence, while respiratory problems were particularly frequent in EA/TEF children without genetic disorders. Colds are more frequent to cause school absence at preschool age, which is in agreement with a high frequency of respiratory disorders in young EA/TEF children [5,26]. As mentioned by parents, school absence may impair social integration with peers, and school achievement. Earlier studies [18,23,27] have shown that EA/TEF children may risk social isolation, a negative effect on relationships and other social functions. This study also raises the question whether school absence may cocontribute to the need for school support. Study limitations include there being no general control group, and restrictions associated with the Swedish setting. It is not clear how families experienced the preschool/school support they received, or if more families wished for school support. Growth impairment may be associated to weakened cognitive performance [11,29]. This and information
M. Dellenmark-Blom et al. / Journal of Pediatric Surgery 53 (2018) 1970–1975
on total duration of anesthetic exposure, neurodevelopmental outcomes, school performance and length of school absence are lacking. Moreover, there is no standardized definition of problematic school absence, and we defined a cutoff for what we term considerable school absence, for use in this study. This should form a focus for future research. Study strengths include a large and fairly representative sample with good response rates and acceptable AUC levels. The Swedish school law ensures the provision of special preschool/school support to children in need [17], and using the total number of study participants in preschool/school benefited the statistical analysis of clinical predictors in agreement with statistical expertise. The need to understand psychosocial consequences after major neonatal surgery has been pointed out [9,11]. This study brings new information to the field. 4. Conclusion Approximately one third of EA/TEF children aged 2–17 years old have special support in preschool/school to help deal with educational or nutritional intake issues. In EA/TEF children without genetic disorders, congenital factors, low birth weight and associated anomalies predict the use of educational support threefold. Surgical characteristics are also related to the use of special preschool/school support. Gastrostomy insertion predicts the use of nutritional intake support fivefold, and major revisional surgery predicts the use of both educational and nutritional support almost eightfold. Special preschool/school support is associated with considerable school absence. This reveals significant health care needs and further stresses the importance of surgical repairs being of good quality, and multidisciplinary follow-up care. Acknowledgment The study was funded by The Queen Silvia Jubilee Foundation, the Sven Jerring Foundation and ALF Grants. References [1] Sfeir R, Piolat C, Lemelle JL, et al. Esophageal atresia: data from a national cohort. J Pediatr Surg 2013;48:1664–9. [2] Pedersen RN, Markow S, Kruse-Andersen S, et al. Esophageal atresia: gastroesophageal functional follow-up in 5-15 year old children. J Pediatr Surg 2013;48:2487–95. [3] Olbers J, Gatzinsky V, Jonsson L, et al. Physiological studies at 7 years of age in children born with esophageal atresia. Eur J Pediatr Surg 2015;25:397–404. [4] Chetcuti P, Phelan PD. Gastrointestinal morbidity and growth after repair of oesophageal atresia and tracheo-oesophageal fistula. Arch Dis Child 1993;68(2):163–6. [5] Chetcuti P, Phelan PD. Respiratory morbidity after repair of oesophageal atresia and tracheooesophageal fistula. Arch Dis Child 1993;68:167–70.
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[6] Malmstrom K, Lohi J, Lindahl H, et al. Longitudinal follow-up of bronchial inflammation, respiratory symptoms, and pulmonary function in adolescents after repair of esophageal atresia with tracheoesophageal fistula. J Pediatr 2008;153:396–401. [7] Lindahl H. Long-term prognosis of successfully operated oesophageal atresia—with aspects on physical and psychological development. Z Kinderchir 1984;39(1):6–10. [8] Bouman NH, Koot HM, Hazebroek FW. Long-term physical, psychological, and social functioning of children with esophageal atresia. J Pediatr Surg 1999;34(3):399–404. [9] Kubota A, Nose K, Yamamoto E, et al. Psychosocial and cognitive consequences of major neonatal surgery. J Pediatr Surg 2011;46(12):2250–3. [10] Faugli A, Bjornland K, Emblem R, et al. Mental health and psychosocial functioning in adolescents with esophageal atresia. J Pediatr Surg 2009;44(4):729–37. [11] Ijsselstijn H, Gischler SJ, Toussaint L, et al. Growth and development after oesophageal atresia surgery: need for long-term multidisciplinary follow-up. Paediatr Respir Rev 2016;19:34–8. [12] Lacher M, Froehlich S, von Schweinitz D, et al. Early and long term outcome in children with esophageal atresia treated over the last 22 years. Klin Padiatr 2010;222 (5):296–301. [13] Hamrick SE, Strickland MJ, Shapira SK, et al. Use of special education services among children with and without congenital gastrointestinal anomalies. Am J Intellect Dev Disabil 2010;115(5):421–32. [14] Legrand C, Michaud L, Salleron J, et al. Long-term outcome of children with oesophageal atresia type III. Arch Dis Child 2012;97:808–11. [15] Mörtlund T. Skolverkets lägesbedömning. Stockholm: Skolverket; 2017. [16] Avdelningen för analys: enheten för förskole- och grundskolestatistik. Särskilt stöd i grundskolan läsåret 2016/17. Stockholm: Skolverket; 2017[8 pp.]. [17] Skollag. 2010:800, Sveriges Riksdag, utbildningsdepartementet regeringskansliet (2010–06-23); 2010. [18] Dingemann C, Meyer A, Kircher G, et al. Long-term health-related quality of life after complex and/or complicated esophageal atresia in adults and children registered in a German patient support group. J Pediatr Surg 2014;49:631–8. [19] Filler RM, Messineo A, Vinograd I. Severe tracheomalacia associated with esophageal atresia: results of surgical treatment. J Pediatr Surg 1992;27:1136–41. [20] Machin D, CM, Walters S. Medical statistics a textbook for the health sciences. Chichester: Wiley; 2007. [21] Flensborg-Madsen T, Mortensen EL. Birth weight and intelligence in young adulthood and midlife. Pediatrics 2017;139(6). https://doi.org/10.1542/peds.2016-3161. [22] Castilloux J, Noble AJ, Faure C. Risk factors for short- and long-term morbidity in children with esophageal atresia. J Pediatr 2010;156:755–60. [23] Dellenmark-Blom M, Chaplin J, Gatzinsky V, et al. Health-related quality of life experiences among children and adolescents born with esophageal atresia: development of a condition-specific questionnaire for pediatric patients. J Pediatr Surg 2016;51 (4):563–9. https://doi.org/10.1016/j.jpedsurg.2015.09.023. [24] Chittmittrapap S, Spitz L, Kiely EM, et al. Anastomotic leakage following surgery for esophageal atresia. J Pediatr Surg 1992;27(1):29–32. [25] Koivusalo AI, Pakarinen MP, Lindahl HG, et al. Revisional surgery for recurrent tracheoesophageal fistula and anastomotic complications after repair of esophageal atresia in 258 infants. J Pediatr Surg 2015;50(2):250–4. [26] Svoboda E, Fruithof J, Widenmann-Grolig A, et al. A patient led, international study of long term outcomes of esophageal atresia: EAT 1. J Pediatr Surg 2018;53(4):610–5. [27] Dellenmark-Blom M, Abrahamsson K, Quitmann JH, et al. Development and pilottesting of a condition-specific instrument to assess the quality-of-life in children and adolescents born with esophageal atresia. Dis Esophagus 2017;30(7):1–9. [28] Dellenmark-Blom M, Chaplin JE, Jönsson L, et al. Coping strategies used by children and adolescents born with esophageal atresia - a focus group study obtaining the child and parent perspective. Child Care Health Dev 2016;42(5):759–67. [29] Aite L, Bevilacqua F, Zaccara A, et al. Short-term neurodevelopmental outcome of babies operated on for low-risk esophageal atresia: a pilot study. Dis Esophagus 2014;27(4):330–4.
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Journal of Pediatric Surgery journal homepage: www.elsevier.com/locate/jpedsurg
Clinical predictors and prevalence of receiving special preschool/school support in children with repaired esophageal atresia Michaela Dellenmark-Blom a,⁎, Linus Jönsson b, Vladimir Gatzinsky b, Kate Abrahamsson a,b a b
Department of Pediatric Surgery, Queen Silvia Children's Hospital, Sahlgrenska University Hospital, 416 85 Gothenburg, Sweden Institute of Clinical Sciences, Department of Pediatrics, Gothenburg University, The Queen Silvia Children's Hospital, 416 86 Gothenburg, Sweden
a r t i c l e
i n f o
Article history: Received 11 September 2017 Received in revised form 21 November 2017 Accepted 22 November 2017 Key words: Esophageal atresia Tracheoesophageal fistula Psychosocial functioning School support Educational support Feeding difficulties
a b s t r a c t Background/purpose: In a sparsely investigated field, we aimed to evaluate the use of special preschool/school support among children with repaired esophageal atresia (EA) and/or tracheoesophageal fistula (TEF), the predicting clinical factors for this support, and level of school absence. Methods: Data on 119 EA/TEF children 2–17 years old were collected through medical records and questionnaires (response rate 95%). Logistical regression analysis identified clinical predictors of special preschool/school support in the population without genetic disorders (n = 105). Nominal hypothesis testing was performed using Fisher's exact test (p b 0.05). Results: Of the 119 children, 35.3% received special preschool/school support; 26.8% educational support, 21.8% support with nutritional intake issues and 13.4% received both types of support. Educational support was independently predicted by birth weight b 2500 g (p = 0.026) and associated anomalies (p = 0.049), nutritional intake support by gastrostomy insertion (p = 0.0028), and both types of supports by major revisional surgery (p = 0.0081). School absence ≥1 month/year, present in 25.5% of the children, was more frequently reported in children receiving preschool/school support, in preschoolers and in those with persistent respiratory problems (p b 0.05). Conclusions: Special preschool/school support is provided for approximately one-third of EA/TEF children. In EA/ TEF children without genetic disorders, use of this support is predicted by congenital and surgical factors, and related to frequent school absence. © 2017 Elsevier Inc. All rights reserved.
Following surgical repair of esophageal atresia (EA) and/or tracheoesophageal fistula (TEF), survival rates now exceed 90% [1], but late morbidity is significant. Dysphagia, gastroesophageal reflux disease [2,3], feeding difficulties [4] and respiratory problems [5,6] such as wheezing, chronic cough, and repeated airway infections may affect children with EA/TEF. Little is, however, known about the psychosocial outcomes. EA/TEF children are reported having both comparable [7] and lower intelligence [8,9] levels than healthy children. Different studies have shown both psychosocial functioning in EA/TEF children to be similar [10] to the general population, but also worse [7–9]. In a literature review from 2016, IJsselstijn et al. [11] concluded that EA/TEF children are at risk of developing school problems. However, this field is
⁎ Corresponding author at: Department of Pediatric Surgery and Urology, The Queen Silvia Children's Hospital, 416 85, Gothenburg, Sweden. Tel.: +46 313434372; fax: +46 31843453. E-mail addresses: [email protected] (M. Dellenmark-Blom), [email protected] (L. Jönsson), [email protected] (V. Gatzinsky), [email protected] (K. Abrahamsson). https://doi.org/10.1016/j.jpedsurg.2017.11.057 0022-3468/© 2017 Elsevier Inc. All rights reserved.
sparsely investigated. In one study [8], 22% of EA/TEF children were in special education (sample ntot = 36, age 8–12 years old) and in another study [10], 33% (sample ntot = 21, age 12–17 years old) of the subjects. In a third study, 10% of children with the condition (sample ntot = 60, primary school-age) attended school for mentally handicapped children [12]. EA/TEF children with associated anomalies, which are present in around 55% [1] of the group, are almost three times more likely to require special education [13], and function more poorly at school, particularly if they have cardiovascular anomalies [14]. Children born with imperforate anus and multiple anomalies (which could include EA), are also more likely to be in special education [13]. To date studies are few [8,10,13,14], include mostly small samples, exclude children of preschool age, and do not properly explain the relationship between clinical factors and school problems. In Sweden, between 5% and 6% of the pupils in elementary school received special educational interventional support, and 1% attended school for children with learning disabilities [15,16], but investigations aiming to describe the school conditions for EA/TEF children are lacking. In this study, we aimed to determine the clinical predictors and prevalence of receiving special preschool/school
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support among children with EA/TEF, and the level of school absence, in a Swedish population. 1. Material and methods 1.1. Patients The study was approved by the regional ethical committee. Parents of children with EA/TEF (Gross A–E) aged 2–17 years, treated between 1997 and 2014 at the Queen Silvia Children's Hospital, Gothenburg, Sweden, were contacted on the phone by a researcher. They received oral information and a study invitation. 137/145 participants accepted written study information, and returned informed consent. 1.2. Data collection The patients' hospital records were reviewed for clinical data up to the time of the study, which included information on neonatal characteristics, surgical treatment(s), associated anomalies/conditions and bronchoscopy results. 130 (94.9%) responded to a standardized postal questionnaire developed by the authors. The first part consisted of sociodemographic and parent/caregiver information (12 questions), and the second part (20 questions) information on the child's age and health status, including five specific questions about the children's preschool/school situation. In Sweden, children attend preschool and preschool-class up six years of age before entering elementary school (grade 1–9) at seven years of age. Upper secondary school (three years) follows after this. The Swedish school law gives all children in preschool/school the right to special school support if needed, preferably delivered in the child's regular class. There are also special schools for children with learning disabilities [15,17]. Families were asked whether the child with EA/TEF attended preschool/school (yes/no), currently had special school support (yes/no), and how frequently the child had been absent from school the previous year (no school absence, one time/year, 2–5 times/year, 6–11 times/year, one time/month, None time/month). The two last questions were followed by open, explorative questions with instructions to parents to further describe the child's special preschool/school support, and list the causes of school absence. A closing question asked parents whether we had omitted to ask any questions which were important to them, and what they were. 1.3. Statistical analysis Statistical analysis was performed using SPSS 22.0 and SAS 9. software. The analysis included 119 children with school attendance (two adolescents dropped out of school, nine families gave no explanation, but seven of these children were younger than for compulsory elementary school). Parents' open answers were categorized into type of preschool/school support and cause of school absence, for evaluation using descriptive statistics (number,%). A priori, we decided to exclude EA/TEF children with genetic disorders from the hypothesis testing. This regarded children with Charge syndrome (n = 5), Apert syndrome (n = 1), Angelman syndrome (n = 1), trisomy 21 and other chromosomal abnormalities (n = 7), with known associations to cognitive, hearing or visual impairments. In the additional sample (n = 105), using predefined hypothesis, univariable logistical regression analysis was performed to identify clinical predictors of special preschool/school support by calculation of odds ratio (OR), 95% confidence interval (CI). The variables included in the models were Neonatal characteristics; child gender, prematurity (gestational age b 37 weeks), low birth weight (b2500 g); Surgery and anesthesia; primary esophageal repair, gastrostomy insertion, any early postoperative complication (recurrent fistula, anastomotic leakage, sepsis, wound infection, pneumothorax with need of drainage, thrombosis), revisional surgery owing to anastomotic leakage or recurrent fistula, N1 anesthesia prior to first hospital discharge, Associated anomalies; associated anomaly, cardiovascular or
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anorectal anomaly, VACTERL association Follow-up; antireflux surgery, dilatation of EA, dilatations of EA N 10 as a criterion for complicated evolution [18], gastrostomy feeding, bronchoscopy-verified severe tracheomalacia/tracheobronchomalacia (an anteroposterior collapse during coughing and expiration documented as ≥75%, excessive and/ or severe [19]), doctor-diagnosed asthma and child-age group at follow-up. Clinical variables resulting in p b 0.1 in the univariable analysis, were included in the multivariable analysis. The significant level for predictors was p b 0.05. The area under the relative (receiver-) operating characteristics (ROC) curve (AUC) was used to estimate the predictor value. AUC N 0.5 is considered acceptable, and AUC of 1.0 equals perfect test [20]. School absence ≥1/month was classed as considerable. We examined whether this was related to specific parent-listed reasons, preschool/school-age and preschool/school support (Fischer's exact test, p b 0.05). 2. Results 2.1. Study population Patient population characteristics (n = 119) are presented in Table 1. 2.2. Prevalence and type of special preschool/school support Out of 119 EA/TEF children, 42 (35.3%) received special preschool/ school support; 32 (26.8%) children used educational support, 9 (7.6%) of whom attended school for children with learning disabilities, and 26 (21.8%) received nutritional intake support. Sixteen (13.4%) EA/TEF children received both educational and nutritional intake support. Following the definitions of special preschool/school support, the prevalence is reported separately for EA/TEF children with genetic disorders (n = 14) and without genetic disorders (n = 105) in Table 2. 2.3. Clinical predictors of special preschool/school support The calculations of OR and AUC in relation to special preschool/ school support in EA/TEF children without genetic disorders (n = 105) are shown in Table 3. The predicting factors of receiving special educational support in the univariable analysis were low birth weight (p = 0.021), N1 anesthesia before first hospital discharge (p = 0.043), associated anomaly (p = 0.042), gastrostomy feeding at follow-up (= 0.0009) and doctor-diagnosed asthma (p = 0.042). Low birth weight (p = 0.026) and associated anomalies (p = 0.049) independently predicted the use of educational support. The predictors of support with nutritional intake issues at preschool/ school in the univariable analysis were gastrostomy insertion (p = 0.0028), revisional surgery owing to anastomotic leakage or recurrent fistula (p = 0.011), associated anomaly (p = 0.031), anti-reflux surgery (p = 0.013), gastrostomy feeding (p = 0.0004), and preschool-age at follow-up (compared to adolescents, p = 0.015). Gastrostomy insertion independently increased the OR by 5.42 (p = 0.0028). The predictors of receiving educational and nutritional intake issues support at preschool/school were revisional surgery owing to anastomotic leakage or recurrent fistula (p = 0.0081) and gastrostomy feeding at follow-up (p = 0.0006) in the univariable analysis, though revisional surgery was the independent predictor (p = 0.0081). 2.4. Level of school absence Information on school absence is shown in Table 4. In EA/TEF children without genetic disorders, school absence ≥1/month was significantly more commonly reported in pupils receiving educational support (47.4% vs 20.28%, p = 0.020), and nutritional intake support (64.7% vs 17.4%, p b 0.001). It was also more common in preschoolers (42.3% vs 19.5%, p = 0.035), and in children with persistent respiratory
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M. Dellenmark-Blom et al. / Journal of Pediatric Surgery 53 (2018) 1970–1975
Table 1 Presentation of the study sample (119 children and their parents). Frequency (%) Child background information Male Gestational week Birth weight (g) Gross A/B/C/D/E Associated anomalies Cardiovascular Gastrointestinal (excluding anorectum) Anorectal Urogenital Limb Vertebral–skeletal Central nervous system Respiratory Eye Ear VACTERL Genetic disorders Primary anastomosis Gastrostomy insertion Number of anesthesia before first hospital discharge Revisional surgery owing to anastomotic leakage or recurrent fistula Follow-up Child age Antireflux surgery Esophageal dilation Gastrostomy feeding at follow-up Doctor-diagnosed asthma Severe tracheomalacia/tracheobronchomalaciaa
a
Median (Min/Max)
36.5 (3.3) 2560 (715)
37 (28/43) 2600 (970/4110)
2.5 (2.5)
2 (1/14)
10 (5)
9 (2–17)
3.4 (11)
0 (0/90)
42 (7)
42 (26/69)
69 (58)
12 (10.1)/6 (5.0)/93 (78.2)/2 (1.7)/6 (5.0) 72 (60.5) 32 (26.9) 9 (7.6) 12 (10.1) 15 (12.6) 9 (7.6) 27 (22.7) 8 (6.8) 4 (3.4) 9 (7.6) 4 (3.4) 19 (16.0) 14 (11.8) 101 (84.9) 43 (36.1) 16 (13.4)
27 (22.7) 49 (41.2) 16 (13.4) 39 (32.8) 18 (15.1)
Parent-report Mother Parental age (years) Highest education university/college Living with cohabitant partner
Mean(SD)
106 (89.1) 59 (49.6) 98 (82.4)
An anteroposterior collapse during coughing and expiration documented as ≥75% [reference [19], excessive and/or severe.
problems (42.3% vs 16.9%, p = 0.014). More preschoolers had school absence ≥ 1/month owing to colds, compared to school-age children (78.6% vs 51.9%, p = 0.015).
2.5. Final open question to parents Five families described additional experiences, as shown in Table 5.
3. Discussion In this study, 35.3% of EA/TEF children received special support in preschool/school. Overall, 26.8% of EA/TEF children received educational support, including 7.6% in a school for children with learning disabilities. Even in EA/TEF children without genetic disorders, the prevalence (18.1%) of educational support seemed higher than in the general Swedish population (5%–6% special educational support)
Table 2 Frequency(%) of special preschool/school support in children with esophageal atresia (EA) and/or tracheoesophageal fistula (TEF). Definition of special school support
SPECIAL SCHOOL SUPPORT
Educational support
School for children with learning disabilities
Support with nutritional intake issues Support with educational & nutritional intake issues
• Educational support, including school for children with learning disabilities • Having support with nutritional intake issues at school • Having a special teacher, school assistant, adjusted learning program, environment or help equipment to support concentration, memory and/or learning • A special school for children with learning disabilities, usually owing to cognitive impairments, who don't achieve the general required school achievement specific to age • Having a teacher/school assistant beside the child during meals for observation or help keeping the correct pace, food consistency, portion sizes, prevent/assist choking episodes or for gaining help with gastrostomy feeding • Jointly having any of the mentioned school supports in the columns educational and nutritional intakes issues
EA, esophageal atresia; TEF, tracheoesophageal fistula. a These patients had major associated malformations.
EA/TEF children with genetic disorders (ntot = 14)
Children with EA/TEF without genetic disorders (ntot = 105)
Number (%)
Number (%)
14 (100)
28 (26.7)
13 (92.9)
19 (18.1)
6 (42.9)
3 (2.9)a
9 (64.3)
17 (16.2)
8 (57.1)
8 (7.6)
Table 3 Calculated odds ratio (OR) and area under the relative (receiver-) operating characteristics curve (AUC) of receiving special educational support in children with esophageal atresia and/or tracheoesophageal fistula (without genetic disorders), using bold text to highlight significant p-values (p b 0.05). EDUCATIONAL SUPPORT
SUPPORT WITH NUTRITIONAL INTAKE ISSUES
Univariable analysis OR (95% CI) NEONATAL CHARACTERISTICS Gender girl Prematurity (GAa b 37 weeks) Low birth weight (b2500 g) SURGERY AND ANESTHESIA No primary esophageal repairb
Any early postoperative complication Revisional surgery owing to anastomotic leakage or recurrent fistula N1 anesthesia before first hospital discharge ASSOCIATED ANOMALIES Associated anomaly Cardiovascular anomaly Anorectal malformation VACTERL association FOLLOW-UP Antireflux surgery Dilatation of EA Dilatations of EA N10 Gastrostomy feeding Broncoscopy verified severe tracheomalacia/tracheobronchomalaciab Doctor-diagnosed asthma
0.8 0.69 (10.29–2.26) 1.66 0.33 (0.60–4.61) 3.37 0.021 (1.20–9.47)
0.53 (0.40–0.65) 0.56 (0.43–0.69) 0.65 3.31 (0.52–0.77) (1.15–9.53)
0.73 (0.15–3.55) 2.58 (0.92–7.29) 1.61 (0.58–4.46) 2.71 (0.80–9.15) 3.22 (1.04–9.99)
Univariable analysis
p-value OR (95% CI) 1.01 (0.35–2.90) 1.43 (0.50–4.07) 1.97 (0.69–5.61)
0.98
0.52 (0.44–0.60) 0.61 (0.48–0.74) 0.56 (0.43–0.69) 0.57 (0.47–0.68) 0.64 (0.52–0.76)
1.50 (0.37–6.07) 5.42 (1.79–16.37) 2.14 (0.73–6.30) 4.79 (1.43–16.06) 2.54 (0.80–8.08)
0.57
3.42 0.042 (1.05–11.13) 2.40 0.099 (0.85–6.78) 0 N/A
0.63 3.35 0.049 (0.53–0.74) (1.00–11.20) 0.59 (0.47–0.72) N/A
1.50 (0.43–5.23)
0.53
0.53 (0.43–0.63)
4.26 (1.14–15.87) 0.82 (0.24–2.77) 2.14 (0.51–9.07) 1.78 (0.50–6.30)
1.43 (0.41–5.06) 0.64 (0.20–2.09) 1.02 (0.98–1.06) 12.77 (2.84–57.46) 1.16 (0.29–4.58) 2.87 (1.04–7.93)
0.58
0.53 (0.41–0.66) 0.55 (0.41–0.69) 0.45 (0.32–0.57) 0.64 (0.53–0.75) 0.51 (0.42–0.60) 0.62 (0.50–0.75)
4.38 (1.36–14.03) 2.54 (0.78–8.25) 1.04 (0.99–1.10) 15.45 (3.37–70.77) 3.25 (0.95–11.16) 2.12 (0.74–6.10)
0.55 (0.41–0.68)
1 0.54 (0.18–1.68) 0.07 (0.01–0.60)
0.69 0.073 0.36 0.11 0.043
0.46 0.30 0.0009 0.84 0.042
0.026
Multivariable analysis
p-value AUC (95% CI) OR (95% CI)
0.51 0.20
0.0028 0.17 0.011 0.11
0.031 0.75 0.30 0.37
0.013 0.12 0.13 0.0004 0.061 0.16
Univariable analysis
p-value OR (95% CI)
Multivariable analysis
p-value AUC (95% CI) OR (95% CI)
0.50 (0.37–0.63) 0.54 (0.41–0.68) 0.58 (0.45–0.72)
1.49 (0.35–6.30) 0.90 (0.20–3.99) 1.62 (0.38–6.88)
0.59
0.53 (0.43–0.63) 0.70 5.42 0.0028 (0.57–0.82) (1.79–16.37) 0.59 (0.46–0.73) 0.63 (0.50–0.75) 0.61 (0.48–0.75)
0.92 (0.10–8.13) 4.05 (0.91–18.10) 2.07 (0.44–9.77) 7.82 (1.71–35.80) 6.07 (0.68–54.01)
0.94
0.65 (0.54–0.76) 0.52 (0.40–0.63) 0.54 (0.44–0.64) 0.54 (0.43–0.65)
2.39 0.30 (0.46–12.43) 1.73 0.48 (0.38–7.76) 0 N/A
0.60 (0.43–0.76) 0.56 (0.37–0.74) N/A
0
N/A
N/A
0.65 (0.51–0.79) 0.61 (0.47–0.75) 0.62 (0.48–0.76) 0.66 (0.54–0.78) 0.59 (0.47–0.71) 0.59 (0.46–0.72)
4.17 (0.78–22.38) 0.29 (0.03–2.71) 1.04 (0.99–1.09) 18.40 (3.52–96.05) 4.25 (0.90–20.10) 3.91 (0.88–17.44)
0.096
0.65 (0.43–0.88) 0.63 (0.43–0.83) 0.46 (0.26–0.65) 0.72 (0.54–0.91) 0.63 (0.44–0.81) 0.66 (0.48–0.85)
0.71 (0.59–0.82)
1 1.64 (0.30–9.15) 0.37 (0.03–4.28)
0.89 0.51
0.067 0.36 0.0081 0.11
0.28 0.087 0.0006 0.068 0.074
p-value
0.55 (0.36–0.74) 0.51 (0.33–0.70) 0.56 (0.37–0.75) 0.50 (0.38–0.63) 0.67 (0.48–0.85) 0.59 (0.39–0.79) 0.69 7.82 0.0081 (0.51–0.88) (1.71–35.80) 0.69 (0.52–0.86)
M. Dellenmark-Blom et al. / Journal of Pediatric Surgery 53 (2018) 1970–1975
Gastrostomy insertion
Multivariable analysis
p-value AUC (95% CI) OR (95% CI)
SUPPORT WITH BOTH EDUCATION AND NUTRITIONAL INTAKE ISSUES
Child age group Preschool age (2–6 years old)c Middle school-age (8–12 years old) Adolescence (13–17 years old)
1 1.52 (0.42–5.54) 1.19 (0.30–4.72)
0.52 0.81
0.29 0.015
0.57 0.42
0.64 (0.47–0.82)
1973
AUC, area under the relative (receiver-) operating characteristics curve; CI, confidence interval; EA, esophageal atresia; GA, gestational age for birth; N/A, not applicable; OR, odds ratio. Event rate in the specific age groups were; Educational support: preschool age (14.8%), middle school age (20.9%), adolescence (17.1%); Nutritional intake support: preschool age (29.6%), middle school age (18.6%), adolescence (2.9%); Both type of supports: preschool age (7.4%), middle school age (11.6%), adolescence (2.9%). a Delayed primary anastomosis/elongation/esophageal replacement. b An anteroposterior collapse during coughing and expiration documented as ≥75%, excessive and/or severe. c Used as reference group for comparison.
1974
M. Dellenmark-Blom et al. / Journal of Pediatric Surgery 53 (2018) 1970–1975
Table 4 Information on school absence among children with esophageal atresia (EA) and/or tracheoesophageal fistula (TEF).
School absence the previous year No school absence 1 time 2–5 times 6–11 times ≥1/month Reasons for school absence Colds General sickness such as just “feeling ill”/gastroenteritis/headache Persistent troublesome respiratory symptoms Examinations and doctor-visits at the hospital Out-clinic visits with physiotherapists or nurses Stomachache Pneumonia GER-related symptoms causing sleeping disorders
EA/TEF children with genetic disordersa
Children with EA/TEF without genetic disordersb
Frequency (%) 0 1 (7.7) 2 (15.4) 4 (30.8) 6 (46.2)
Frequency (%) 10 (9.8) 6 (5.9) 37 (36.3) 23 (22.5) 26 (25.5)
6 (46.2)
62 (60.8)
4 (30.8)
29 (28.4)
1 (7.7) 10 (76.9) 5 (38.5) 1 (7.7) 0 3 (23.1)
20 (19.6) 16 (15.7) 6 (5.9) 5 (4.9) 4 (3.9) 3 (2.9)
EA, esophageal atresia; GER, gastro-esophageal reflux; TEF, tracheoesophageal fistula. a One missing information because the child started school during the previous year, calculated on the basis of information gained from 13 children. b Three missing information, calculated on the basis of information gained from 102 children.
[15,16], but slightly lower (22–33%) than indicated in previous studies of EA/TEF children [8,10]. However, the definitions of educational school support and the study populations (i.e. preschool, secondary school) may vary. In agreement with the Hamrick et al. study [13] we found an increased use of special educational support in EA/TEF children with associated anomalies. Impaired school-functioning has been found particularly in EA/TEF children with cardiovascular anomalies [14]. In this study, cardiovascular, anorectal anomalies or VACTERL association did not increase the special preschool/school support. One possible explanation is that sample sizes become smaller when investigating the impact of different types of anomalies. The variable N 1 anesthesia before first hospital discharge, did predict educational support in the univariable analysis, but was not an independent predictor. A possible explanation is that this variable might be a proxy for higher level of morbidity in the EA/TEF patient. In our study sample, the most common reasons for several anesthesias were gap measurements, esophageal dilatation, revisional surgery of EA/TEF repair, gastrostomy insertions, antireflux surgery and broncoscopy examinations needed owing to airway disease. Low birth weight independently predicted use of educational support. Low birth weight and prematurity are interrelated and may extend the neonate's need for mechanical ventilation. This, in turn may increase the risk of poorer neurodevelopmental outcomes, and explain such findings. However, in this study, prematurity, postoperative complications or revisional surgery (associated with possible prolonged mechanical ventilation) did not significantly affect the educational support. Low birth weight (controlled for possible relevant confounders) has been associated with lower intelligence in the general population continuing into late adulthood [21]. This, in common with anomalies described in our study, would support a hypothesis of factors related to fetal development and to the malformation. In comparison, normal intelligence has been demonstrated in EA/TEF children without significant associated anomalies [7]. Several surgical variables predicted use of nutritional intake support in EA/TEF children. Gastrostomy insertion may be required for reasons such as “long-gap EA”, revisional surgery, cyanotic spells, severe GER, or associated anomalies. Some of these indications may vary between centers. Additionally to “long-gap EA”, the main indications for
Table 5 Comments added by five families of children with esophageal atresia (EA) and/or tracheoesophageal fistula (TEF) in explorative questions regarding aspects of importance to them. The child experienced school as hard/demanding The child had difficulties Parents (n = 2) of adolescent boys managing the grades Parents (n = 4), three parents of 2–6 year Prolonged school absence affected social integration and/or old children and one parent of a school achievement teenage boy Parents (n = 3) of children Respiratory symptoms caused 2–6 years old prolonged school absence Repeated needs of hospital admissions One parent of a teenage boy caused prolonged school absence Frequent school absence owing to One parent of a preschool girl misunderstanding of vomiting as gastroenteritis by teachers Parents (n = 2) of adolescent boys
EA, esophageal atresia; TEF, tracheoesophageal fistula.
gastrostomy insertion at our center were severe nutrition difficulties, severe GER or severe tracheomalacia, with risk of failure to thrive. Although the majority of gastrostomies are temporary, a prior insertion may imply a more complex clinical course. Feeding difficulties are a known consequence of EA/TEF repair [4], and gastrostomy may inhibit the development of normal eating behavior. This, and the underlying morbidity, can explain why a prior gastrostomy insertion may influence the need for nutritional intake support at preschool/school. Interestingly, revisional surgery for anastomotic leakage or recurrent fistula independently predicted special preschool/school support for both educational and nutritional issues. Although major revisional surgery is regarded as a criterion for severe EA/TEF [18,22,23], the impact on future sequelae is only partly understood. Anastomotic leakage is associated with stricture development [24]. In this study, esophageal dilatation was not a predictor of special preschool/school support. In the Koivusalo et al. study [25], 42 (16%) EA/TEF patients underwent revisional surgery, and in 92% of the survivors, patients eventually resumed full oral intake. This study suggests that major revisional surgery is associated with significant health care needs in EA/TEF children, necessitating support at preschool/school age. The trend toward higher levels of nutritional intake support among preschoolers with EA/TEF could be explained by feeding difficulties having less impact with increased age [4]. However, this is contradicted by another study [26], and from quality-of-life-studies, suggesting that eating issues may affect EA/TEF children across childhood [23,27]. Another explanation is the development of coping strategies with increased age, which help EA/TEF children to independently deal with nutritional intake issues [28]. No study has previously reported on the relationship between special preschool/school support and school absence in EA/TEF children. In EA/TEF children with genetic disorders health care visits seemed to be the primary cause of school absence, while respiratory problems were particularly frequent in EA/TEF children without genetic disorders. Colds are more frequent to cause school absence at preschool age, which is in agreement with a high frequency of respiratory disorders in young EA/TEF children [5,26]. As mentioned by parents, school absence may impair social integration with peers, and school achievement. Earlier studies [18,23,27] have shown that EA/TEF children may risk social isolation, a negative effect on relationships and other social functions. This study also raises the question whether school absence may cocontribute to the need for school support. Study limitations include there being no general control group, and restrictions associated with the Swedish setting. It is not clear how families experienced the preschool/school support they received, or if more families wished for school support. Growth impairment may be associated to weakened cognitive performance [11,29]. This and information
M. Dellenmark-Blom et al. / Journal of Pediatric Surgery 53 (2018) 1970–1975
on total duration of anesthetic exposure, neurodevelopmental outcomes, school performance and length of school absence are lacking. Moreover, there is no standardized definition of problematic school absence, and we defined a cutoff for what we term considerable school absence, for use in this study. This should form a focus for future research. Study strengths include a large and fairly representative sample with good response rates and acceptable AUC levels. The Swedish school law ensures the provision of special preschool/school support to children in need [17], and using the total number of study participants in preschool/school benefited the statistical analysis of clinical predictors in agreement with statistical expertise. The need to understand psychosocial consequences after major neonatal surgery has been pointed out [9,11]. This study brings new information to the field. 4. Conclusion Approximately one third of EA/TEF children aged 2–17 years old have special support in preschool/school to help deal with educational or nutritional intake issues. In EA/TEF children without genetic disorders, congenital factors, low birth weight and associated anomalies predict the use of educational support threefold. Surgical characteristics are also related to the use of special preschool/school support. Gastrostomy insertion predicts the use of nutritional intake support fivefold, and major revisional surgery predicts the use of both educational and nutritional support almost eightfold. Special preschool/school support is associated with considerable school absence. This reveals significant health care needs and further stresses the importance of surgical repairs being of good quality, and multidisciplinary follow-up care. Acknowledgment The study was funded by The Queen Silvia Jubilee Foundation, the Sven Jerring Foundation and ALF Grants. References [1] Sfeir R, Piolat C, Lemelle JL, et al. Esophageal atresia: data from a national cohort. J Pediatr Surg 2013;48:1664–9. [2] Pedersen RN, Markow S, Kruse-Andersen S, et al. Esophageal atresia: gastroesophageal functional follow-up in 5-15 year old children. J Pediatr Surg 2013;48:2487–95. [3] Olbers J, Gatzinsky V, Jonsson L, et al. Physiological studies at 7 years of age in children born with esophageal atresia. Eur J Pediatr Surg 2015;25:397–404. [4] Chetcuti P, Phelan PD. Gastrointestinal morbidity and growth after repair of oesophageal atresia and tracheo-oesophageal fistula. Arch Dis Child 1993;68(2):163–6. [5] Chetcuti P, Phelan PD. Respiratory morbidity after repair of oesophageal atresia and tracheooesophageal fistula. Arch Dis Child 1993;68:167–70.
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