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. Author manuscript; available in PMC: 2026 Apr 16.
Published in final edited form as: Birth Defects Res. 2022 Oct 19;115(1):96–109. doi: 10.1002/bdr2.2104

School Age Educational Outcomes of Infants Born with Congenital Diaphragmatic Hernia

Alyssa R Walden a,b,*, Wendy N Nembhard a,c,d, Chary Akmyradov e, Anthony Goudie f, Nahed O ElHassan a,d
PMCID: PMC13082199  NIHMSID: NIHMS2158826  PMID: 36260492

Abstract

Background

To compare academic proficiency among children with congenital diaphragmatic hernia (CDH) versus controls and identify predictors of academic performance among children with CDH.

Methods

Infants born with CDH in Arkansas, 2000-2005, were identified from the Arkansas Reproductive Health Monitoring System. For each case, two controls were selected from birth certificate data and matched for hospital and month of birth, sex, and race/ethnicity. Data on re-hospitalization within the first 5 years and payer data were collected from the Arkansas Hospital Inpatient Discharge Database. Surviving cases and controls were linked to the Arkansas Department of Education database. Primary outcomes were odds of proficiency on fourth grade literacy and mathematics achievement tests. Multivariable logistic regression models evaluated the association between study characteristics and academic proficiency.

Results

The final study cohort included 25 surviving CDH cases and 31 controls who were linked to their education data. After adjusting for differences in characteristics (5-minute Apgar score and associated congenital anomalies) between cases and controls, there were no statistically significant differences in literacy (72% vs. 84%, P=0.93) or mathematics (64% vs. 81%, P=0.98) test proficiency between the two groups. In multivariable analyses, among CDH cases, oxygen at discharge and Medicaid payer/longer hospital stay were associated with worse fourth grade literacy and mathematics proficiency, respectively.

Conclusions

Oxygen at discharge, Medicaid payer, and longer hospital stay were associated with lower academic performance among CDH cases.

Keywords: CDH, educational outcomes, neurodevelopmental outcomes, school age outcomes

INTRODUCTION

Congenital diaphragmatic hernia (CDH) is an anatomical congenital anomaly in which a defect in the diaphragm gives way to herniation of the abdominal contents into the intrathoracic cavity. CDH is estimated to occur in approximately 1 in 3,000 live births (Wynn, Krishnan, et al., 2013). Through the evolution and standardization of treatment strategies, more CDH patients are surviving the acute neonatal period (Bagolan & Morini, 2007; Doyle & Lally, 2004), which can lead to long-term comorbidities such as the continued need for supplemental oxygen and chronic lung disease, along with other complications such as failure to thrive, and neurodevelopmental delays (ND) (Chiu & IJsselstijn, 2012; Jaillard et al., 2003; Peetsold et al., 2008). Over time, these chronic comorbidities ultimately lead to increased healthcare utilization, particularly for infants with CDH requiring extracorporeal membrane oxygenation (ECMO) (Pawlik et al., 2009; Putnam et al., 2016). The growing number of CDH patients surviving into adulthood with various chronic health conditions, along with increases in their healthcare expenditures, underscore the importance of evaluating their long-term outcomes and quality of life (Lemacks et al., 2013). ND impairment has repeatedly been described as a significant comorbidity among CDH survivors (Danzer &Hedrick, 2011; Wynn, Krishnan, et al., 2013; Morini et al., 2017). However, the majority of previously published ND studies of CDH patients focused on early ND outcomes (12 - ≤ 36 months) (Bernbaum et al., 1995; D’Agostino et al., 1995; NINOS, 2000; Jaillard et al., 2003; Chen et al., 2007; Friedman et al., 2008; Danzer et al. 2010, 2013; Wynn, Aspelund, et al. 2013; Antiel et al., 2017; Kim et al., 2021). Studies that examined their outcomes at preschool (>36 months to ≤5 years) (Rasheed et al., 2001; Danzer et al., 2017) through school age and on to adolescence (ages 6-19 years) (Rasheed et al., 2001; Jakobson et al., 2009; Bouman et al., 2000; Tureczek et al., 2012; Benjamin et al., 2013; Madderom et al., 2012; Frisk et al., 2011), largely utilized aptitude tests such as the Wechsler Intelligence Scale for Children or relied on questionnaires and parental recall of the student’s school performance and competencies (Peetsold et al., 2009; Ost et al., 2018; Morsberger et al., 2019). Despite being commonly referenced, aptitude tests are limited in their ability to predict longer-term ND outcomes (Hack, 2005; Danzer et al., 2017). Conversely, there is evidence suggesting that school age standardized achievement test scores are better predictive of future educational attainment in adulthood (Ritchie & Bates, 2013).

Thus, we aimed to evaluate school academic performance on achievement tests of children born with CDH in Arkansas (2000-2005) compared to unaffected controls and to identify neonatal and maternal predictors of academic proficiency among these children. We hypothesized, a priori, that children born with CDH would have lower academic performance compared to unaffected controls.

METHODS

Design and Linkage between Databases

The study received the Arkansas Department of Health Scientific Advisory Committee and University of Arkansas for Medical Sciences Institutional Review Board approval and waiver of informed consent. Patients born with CDH from January 1, 2000 through December 31, 2005 were identified from the Arkansas Reproductive Health Monitoring System, a statewide birth defects registry that monitors for diagnoses of a structural congenital malformation during pregnancy, after stillbirth or termination of pregnancy, after live birth, and up to 2 years of age. CDH patients who were either stillborn, died in infancy, or childhood, were identified through linkage between the Arkansas Reproductive Health Monitoring System and the Arkansas Department of Health Vital Health Records databases. Initially, two controls were randomly selected from the birth certificate database based on hospital and month of birth, race/ethnicity, and sex. However, cases and controls who did not survive to school age or could not be linked to their educational data were excluded from the final analysis. While cases and controls were selected based on birth information, controls were subject to independent forms of attrition. Accordingly, the case-control link is not used in this study, but controls are still utilized as a comparison group. Limited clinical variables, demographic and socioeconomic characteristics including maternal race, marital status, and education were extracted for cases and controls from the Arkansas birth certificates (Table 1). Additional clinical variables of surviving CDH cases were collected from the medical records at Arkansas Children’s Hospital, the state’s only level IV neonatal intensive care unit and pediatric specialty-care facility, where infants born with CDH in Arkansas were typically transferred after birth. Data abstracted from the medical records included birth history, details of operative repair, postoperative complications, respiratory and ECMO support, length of initial hospitalization, duration of oxygen support, and feeding route at time of discharge (Table 2). Sex and gestational age specific growth curves based on U.S. data were used to delineate appropriate, small, and large for gestational age infants (birthweight ≥10th- ≤90th, <10th, and >90th percentile for gestational age, respectively) (Olsen et al., 2010). With permission from the Scientific Advisory Committee at the Arkansas Department of Health, the birth certificate number was used to link data from the Arkansas Department of Health to the Arkansas Hospital Inpatient Discharge database. This database included a unique personal identifier that allowed the linkage of a person across years and hospitalizations lasting ≥1 day. Re-hospitalization data (length of stay, procedures, and discharge diagnoses) within the first 5 years of life, along with healthcare payer type, were then collected on CDH cases. We considered healthcare payer type and maternal education as proxies of socioeconomic status. The combined dataset containing surviving cases and controls was then securely transferred to the Arkansas Department of Education, where scores were retained from the Arkansas Augmented Benchmark Examination in literacy and mathematics, an annual achievement test taken by students who attend public school in Arkansas during third through eighth grade. These achievement test scores were based on scaled scores of 0 to 1000 and were assigned according to the percentage of correct answers (Division of Elementary and Secondary Education - Offices - Learning Services - Assessment: Archived Assessment Materials, n.d.). Students who attended private school, were home schooled, moved out of Arkansas, or had significant cognitive delays, did not sit for the Benchmark Examination and were therefore excluded from analysis. The literacy and mathematics standardized test scores were designated each academic year by the Arkansas Department of Education into 4 categories: advanced, proficient, basic, or below basic based on the percentage of questions answered correctly (Division of Elementary and Secondary Education, n.d.). Students were considered “proficient” and “non-proficient” if their scores were designated as proficient or advanced and basic or below basic on the literacy or mathematics benchmark examination, respectively (ElHassan et al., 2018). The primary outcome measures were the adjusted odds of attaining proficiency on fourth grade literacy and mathematics achievement tests (Elhassan et al., 2022; Kaiser et al., 2015). We elected to evaluate fourth grade achievement test proficiency as our primary outcome, because students were first introduced to the Benchmark Examination during their third grade school year and therefore would have been previously acquainted with the standardized testing process. In addition, multiple previous studies have linked perinatal characteristics with fourth grade standardized test results and school performance at ages 8 to 11 years (ElHassan et al., 2021; Hutchinson et al., 2013; Johnson et al., 2009; Kaiser et al., 2015; Kirkegaard et al., 2006; Mulkey et al., 2016).

Table 1.

Maternal and Infant Characteristics for Infants Born with Congenital Diaphragmatic Hernia (Cases) and Infants Born without Structural Birth Defects (Controls) in Arkansas, 2000-2005†

Characteristics Cases Linked to
Education Data
N= 25		 Controls Linked to
Education Data
N= 31		 P-Value
Maternal characteristics
Age (years), mean (SD) 27 (6) 25 (5) 0.27
Parity, n (%) 0.05
 0-3 25 (100) 29 (94)
Race/Ethnicity, n (%) 0.65
 Hispanic and Non-Hispanic black 3 (12) 2 (6)
 Non-Hispanic white 22 (88) 29 (94)
Any prenatal care (yes), median (IQR) 12 (9, 15) 11 (9, 13) 0.91
Maternal cigarette smoking during pregnancy (yes), n (%) 9 (36) 7 (23) 0.30
Married (yes), n (%) 15 (60) 21 (68) 0.55
Maternal education, n (%) 0.74
 High school or greater 21 (84) 24 (77)
Neonatal characteristics
Male, n (%) 14 (56) 19 (61) 0.69
Birth weight (g), mean (SD) 3298 (601) 3253 (394) 0.75
Gestational age (weeks), mean (SD) 38 (2) 39 (2) 0.21
 Missing 1 0
Size for gestation, n (%) 0.52
 SGA 3 (13) 2 (7)
 AGA 19 (79) 28 (90)
 LGA 2 (8) 1 (3)
 Missing 1 0
Singleton, n (%) 24 (96) 31 (100) 0.45
5-minue Apgar score <7, n (%) 9 (36) 0 (0) 0.0003
Vaginal delivery, n (%) 18 (72) 24 (77) 0.64
Presence of other congenital anomalies‡, n (%) 3 (12) 0 (0) <0.0001
Healthcare payer type, n (%) 0.75
 Medicaid or self-pay 10 (40) 12 (44)
 Private 15 (60) 15 (56)
 Missing 0 4
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†

Only patients who were successfully linked to their achievement tests scores are shown in this table

‡

Congenital heart disease diagnoses of atrial and ventral septal defects, and a renal anomaly.

Abbreviations: AGA, appropriate for gestational age (birth weight 10th - 90th percentile); IQR, interquartile range; LGA, large for gestational age (birth weight > 90th percentile); SD, standard deviation; SGA, small for gestational age (birth weight <10th percentile). Statistics: Means and medians of variables were compared using T-tests and Mann-Whitney U test, respectively. Categorical variables were evaluated using Chi-square or Fisher's Exact tests.

Table 2.

Maternal and Infant Characteristics of Infants Born with Congenital Diaphragmatic Hernia in Arkansas (2000-2005)†

Characteristics Total Patients with
CDH
(N=42)		 CDH linked to
education data
(N=25)		 CDH not linked to
education data
(N=17)		 P-Value
Maternal characteristics
Mean maternal age (years), mean (SD) 26 (6) 27 (6) 26 (6) 0.75
Parity, n (%) 0.66
 0-1 28 (67) 16 (64) 12 (71)
Race/Ethnicity, n (%) 0.67
 Hispanic and Non-Hispanic black 6 (14) 3 (12) 3 (18)
 Non-Hispanic white 36 (86) 22 (88) 14 (82)
Any prenatal care (yes), median (IQR) 11 (9, 15) 12 (9, 15) 10 (10, 14) 0.96
 Missing 2 0 2
Smoking (yes), n (%) 11 (26) 9 (36) 2 (12) 0.15
Married (yes), n (%) 26 (62) 15 (60) 11 (65) 0.76
Maternal education, n (%) 1.00
 High school or greater 36 (86) 21 (84) 15 (88)
Neonatal characteristics
Male, n (%) 24 (57) 14 (56) 10 (59) 0.86
Birth weight (g), mean (SD) 3260 (553) 3298 (601) 3204 (484) 0.59
Gestational age (weeks), mean (SD) 38 (2) 38 (2) 38 (2) 0.88
 Missing 1 1 0
Size for gestation, n (%) 0.47
 SGA 3 (7) 3 (13) 0 (0)
 AGA 34 (83) 19 (79) 15 (88)
 LGA 4 (10) 2 (8) 2 (12)
 Missing 1 1 0
Vaginal delivery, n (%) 29 (69) 17 (68) 12 (71) 0.86
Singleton, n (%) 41 (98) 24 (96) 17 (100) 1.00
5-minue Apgar score <7, n (%) 16 (38) 9 (36) 7 (41) 0.73
Prenatal diagnosis (yes), n (%) 11 (27) 7 (28) 4 (25) 1.00
 Missing 1 0 1
Associated congenital anomalies (yes), n (%) 0.47
 Congenital heart disease‡ 3 (7) 2 (8) 1 (6)
 Renal 1 (2) 1 (4) 0 (0)
 None 38 (90) 22 (88) 16 (94)
Defect location, n (%) 0.11
 Left 33 (79) 17 (68) 16 (94)
 Right 8 (19) 7 (28) 1 (6)
 Bilateral 1 (2) 1 (4) 0 (0)
Hernia type 0.48
 Bochdalek 32 (86) 19 (83) 13 (93)
 Morgagni 3 (8) 3 (13) 0 (0)
 Total 2 (5) 1 (4) 1 (7)
 Missing 5 2 3
Days of life at first surgical repair, median (IQR) 2 (1, 6) 2 (1, 7) 2 (1, 5) 0.70
 Missing 1 0 1
Repair with patch, n (%) 16 (38) 10 (40) 6 (35) 0.76
Intrathoracic liver, n (%) 16 (41) 12 (52) 4 (25) 0.09
 Missing 3 2 1
Hernia sac present (yes), n (%) 10 (24) 6 (24) 4 (25) 1.00
 Missing 1 0 1
ECMO, n (%) 14 (33) 9 (36) 5 (29) 0.66
 Surgical repair on ECMO, n (%) 11 (79) 7 (78) 4 (80) 1.00
Duration of ECMO support (days), median (IQR) 12 (6, 15) 10 (6, 13) 12 (12, 23) 0.25
Oxygen requirement at 30 DOL, n (%) 16 (44) 11 (46) 5 (42) 0.81
 Missing 6 1 5
Oxygen requirement at discharge, n (%) 13 (32) 8 (32) 5 (31) 0.96
 Missing 1 0 1
Feeding route at discharge, n (%) 0.57
 PO 29 (69) 16 (64) 13 (76)
 Nasogastric tube (with or without PO supplementation) 7 (17) 5 (20) 2 (12)
 Gastrostomy tube (with or without PO supplementation) 6 (14) 4 (16) 2 (12)
Length of index hospitalization (days), median (IQR) 26 (10, 58) 28 (15, 47) 16 (10, 58) 0.67
Re-hospitalization in the first 5 years of life, n (%) 19 (45) 14 (56) 5 (29) 0.09
 Surgical 10 (53) 7 (50) 3 (60) 1.00
 Medical 16 (84) 13 (93) 3 (60) 0.15
 Missing 1 0 1
Healthcare payer type, n (%) 0.94
 Medicaid/self-pay 17 (40) 10 (40) 7 (41)
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†

Numbers that do not add up to the total are a result of missing observations/values

‡

Congenital heart disease diagnoses included atrial and ventral septal defects.

Abbreviations: AGA, appropriate for gestational age (birth weight 10th - 90th percentile); CDH, congenital diaphragmatic hernia; DOL, days of life; ECMO; extracorporeal membrane oxygenation; IQR, interquartile range; LGA, large for gestational age (birth weight > 90th percentile); PO, by mouth; SD, standard deviation; SGA, small for gestational age (birth weight <10th percentile).

Statistics: Means and medians of variables were compared using the T-test and Mann-Whitney U tests, respectively. Categorical variables were evaluated using Chi-square or Fisher's Exact tests.

Statistical Analysis

Chi-square/Fisher's exact and Mann-Whitney U/T-Tests were used to evaluate descriptive characteristics between CDH cases and controls and between proficient/non-proficient CDH cases. Raw test scores from the state along with the number of students from each public school were utilized to estimate the mean and standard deviation for each testing year. The means and standard deviations were then used to standardize each testing year’s proficiency threshold score to obtain z-scores for both the mathematics and literacy benchmark exam. Year adjusted z-scores were obtained by subtracting the state z-score from each student’s z-score and dividing by the state standard deviation by each school year. Bivariate analyses were completed to compare the characteristics of CDH cases who were proficient versus non-proficient on achievement tests. Multicollinearity was evaluated using a variance inflation factor and Pearson correlation coefficients. Variable cluster analysis was used to examine and eliminate correlated variables. Variables with P ≤0.2 on bivariate analyses were included in multivariable logistic regression models using a stepwise approach in order to evaluate associations between neonatal/maternal characteristics and academic proficiency. Firth penalized likelihood regression was performed to model literacy proficiency due to small number of observations. However, maximum likelihood was rather used to model mathematics proficiency since Firth regression did not perform well in this analysis. Model validity was measured using the area under the curve (AUC). All calculations were performed using SAS v.9.4 (SAS Institute Inc., Cary, NC, USA).

RESULTS

Study Cohort

Of the 63 infants born with CDH, 21 patients did not survive infancy (Supplemental Table 1). All surviving CDH infants (n=42) were transferred to Arkansas Children’s Hospital shortly after birth. Cases and controls who did not survive to school age or could not be linked to their educational data were excluded from analysis (Figure 1).

Fig. 1. Diaphragmatic Hernia Cases and Controls Linked through Multiple Databases.

Fig. 1.

Fig. 1.

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†Includes CDH cases who were born in Arkansas and transferred to Arkansas Children’s Hospital, the state’s only level IV neonatal intensive care unit.

‡Controls who died or could not be linked to their educational outcomes were excluded from analysis. 31 controls were ultimately linked to their achievement test scores.

§Students who attended private school, were home schooled, moved out of Arkansas, or had significant cognitive delays, did not sit for the Benchmark Examination and were therefore excluded from analysis.

Abbreviations: ADE, Arkansas Department of Education; ADH, Arkansas Department of Health; AHID, Arkansas Hospital Inpatient Discharge; CDH, Congenital Diaphragmatic Hernia.

Cohort Characteristics

The mean gestational age and birthweight of CDH survivors was 38 weeks and 3260 g, respectively (Table 2). Sixty percent of CDH survivors (25/42) were successfully linked to their educational records. No significant differences were detected in demographic, clinical, or socioeconomic variables between the CDH patients who were linked versus not linked to their educational data (Table 2). The majority of the cohort (86%) were Non-Hispanic white. Almost 80% (33/42) of cases were diagnosed with a left-sided diaphragmatic defect and 41% (16/39) had an intrathoracic liver. One-third of cases (14/42) required venoarterial ECMO support for a median of 12 days (Interquartile Range [IQR], 6-15). Four pediatric surgeons performed an approximately equal number of CDH repairs during the study period, with a median time of first operative repair at two days of life (IQR, 1-6). Almost one third (13/41) of CDH survivors were oxygen dependent at time of hospital discharge. In addition, 45% (19/42) of these patients were re-hospitalized within the first five years of life. The most common etiologies for hospital readmission were pulmonary related complications such as bronchiolitis or pneumonia. A higher proportion of CDH cases, compared to controls, had a 5-minute Apgar score <7 (36% vs. 0%, P=0.0003) and associated congenital anomalies (12% vs. 0%, P<0.0001) (Table 1).

Educational Outcomes

While CDH survivors were less proficient than controls on literacy (72% vs. 84%, P=0.30) and mathematics achievement tests (64% vs. 81%, P=0.18), the difference was not statistically significant (Table 3). Even after adjusting for differences in 5-minute Apgar scores and associated congenital anomalies, the results remained unchanged on the literacy and mathematics achievement tests respectively (Adjusted Odds Ratio (aOR)=0.93; 95% CI 0.18-5.97; P=0.93; aOR=0.98; 95% CI 0.21-5.46; P=0.98) (Table 3). After standardizing for differences in each testing year’s proficiency, the z-scores for both the literacy and mathematics benchmark exams were also not statistically significant (Literacy −0.37(0.39), P=0.36; Mathematics −0.58(0.39), P=0.14).

Table 3.

Comparison of Fourth Grade Literacy and Mathematics Proficiency between CDH Cases and their Controls

Education Data Proficiency
of Cases
Linked to
Educational
Data
N= 25		 Proficiency
of Controls
Linked to
Educational
Data
N= 31		 Unadjusted
OR (95% CI)		 Unadjusted
P-Value		 Adjusted
OR (95% CI)		 Adjusted
P-Value
Literacy achievement test, n (%) 18 (72) 26 (84) 0.51 (0.14, 1.77) 0.30 0.93 (0.18, 5.97) 0.93
Mathematics achievement test, n (%) 16 (64) 25 (81) 0.44 (0.13, 1.41) 0.18 0.98 (0.21, 5.46) 0.98
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Abbreviations: CI, confidence interval; OR, odds ratio; SD, standard deviation

Statistical Analysis: Logistic Regression was used to model the proficiency test results. Unadjusted P-values were obtained with observations being case/control as main predictor variable. Adjusted P-values were obtained using main predictor variable case/control, and confounders Apgar<7, and any associated anomalies.

Multivariate Analysis of CDH Cases Based on Academic Proficiency

On bivariate analyses, CDH patients who were delivered via vaginal compared to cesarean delivery, had nine times the odds of attaining proficiency on the fourth grade literacy achievement test (OR=9.74; 95% CI 1.35-70.39; P=0.02) (Table 4). In addition, CDH patients who required supplemental oxygen at 30 days of life (OR=0.13; 95% CI 0.02-0.85; P=0.03) and those who were discharged home on supplemental oxygen (OR=0.10; 95% CI 0.01-0.74; P=0.02), were less likely to reach proficiency on their fourth grade mathematics and literacy achievement test, respectively. In multivariable regression analysis, multicollinearity was evaluated using variance inflation factor and Pearson correlation coefficient. For literacy proficiency outcome, 30 day oxygen requirement and oxygen requirement at discharge were collinear. Oxygen requirement at discharge was preferentially utilized since it performed better in the model. For mathematics proficiency outcome, variable cluster analysis was additionally performed in order to reduce variables due to collinearity. As a result, ECMO, 30 day oxygen requirement, oxygen requirement at discharge, exclusively PO feeding at discharge were removed from final analysis. In multivariable regression analysis, CDH survivors who had a private compared to public healthcare payer type were 24 times more likely to be proficient in mathematics (aOR=23.6; 95% CI 1.04-532.79; P=0.05). With each additional day of hospital stay, CDH survivors were 6% less likely to be proficient in mathematics (aOR=0.94; 95% CI 0.89-1.00; P=0.04). The AUC of the mathematics model was estimated at 0.91(95% CI 0.74-1.00). However, these estimates could be imprecise due to the small sample size of 25 and multiple explanatory variables.

Table 4.

Bivariate Analysis of Proficiency on Fourth Grade Literacy and Mathematics Achievement Tests among CDH Survivors

Characteristics Proficiency on Fourth Grade Literacy
Achievement Test		 Proficiency on Fourth Grade
Mathematics Achievement Test
OR (95% CI) P-Value OR (95% CI) P-Value
Maternal characteristics
Age (years) 0.89 (0.74, 1.06) 0.18* 0.98 (0.84, 1.13) 0.74
Parity 0.65 0.87
 2-3 Reference Reference
 0-1 1.50 (0.26, 8.72) 0.87 (0.16, 4.77)
Race/Ethnicity 0.74 0.33
 Hispanic and Non-Hispanic Black Reference Reference
 Non-Hispanic White 1.52 (0.12, 18.84) 3.44 (0.28, 42.02)
Any prenatal care 0.83 0.21
 No Reference Reference
 Yes 1.01 (0.89, 1.16) 1.12 (0.94, 1.33)
Smoking 0.65 0.53
 No Reference Reference
 Yes 0.67 (0.12, 3.90) 0.59 (0.11, 3.14)
Married 0.53 0.27
 No Reference Reference
 Yes 0.56 (0.09, 3.48) 2.56 (0.48, 13.63)
Education 0.99 0.55
 Less than high school Reference Reference
 High school or greater 1.02 (0.10, 10.56) 1.93 (0.22, 16.72)
Neonatal characteristics
Infant sex 0.39 0.97
 Female Reference Reference
 Male 0.46 (0.07, 2.80) 1.04 (0.20, 5.31)
Birth weight (g) 1.00 (1.00, 1.00) 0.79 1.00 (1.00, 1.00) 0.46
Gestational age at birth (week) 1.10 (0.60, 2.01) 0.77 1.05 (0.60, 1.85) 0.86
AGA 0.32 0.60
 No Reference Reference
 Yes 0.19 (0.01, 5.19) 0.56 (0.06, 5.15)
Delivery mode 0.02* 0.09*
 Cesarean section Reference Reference
 Vaginal delivery 9.74 (1.35, 70.39) 4.72 (0.78, 28.41)
Plurality 0.91 0.45
 Twin Reference Reference
 Singleton 0.76 (0.01, 78.30) 5.92 (0.06, 601.83)
Apgar score at 5 minutes 0.65 0.16*
 ≥7 Reference Reference
 <7 0.67 (0.12, 3.90) 0.30 (0.05, 1.65)
Known prenatal diagnosis of CDH 0.46 0.66
 No Reference Reference
 Yes 2.25 (0.27, 19.02) 0.67 (0.11, 3.98)
Associated congenital anomalies 0.50 0.38
 No Reference Reference
 Yes 0.30 (0.01, 10.13) 0.20 (0.01, 6.90)
Defect location 0.62 0.74
 Right Reference Reference
 Left 1.36 (0.20, 9.48) 0.80 (0.12, 5.27)
 Bilateral 0.13 (0.001, 19.00) 0.15 (0.001, 18.40)
Hernia Type 0.65 0.79
 Total Reference Reference
 Bochdalek 8.02 (0.08, 840.03) 5.07 (0.05, 523.48)
 Morgagni 5.07 (0.03, 837.77) 5.07 (0.03, 839.31)
Days of life at first surgical repair (d) 1.00 (0.98, 1.02) 0.78 1.01 (0.98, 1.03) 0.64
Operative repair 0.08* 0.07*
 Primary Reference Reference
 Patch 0.19 (0.03, 1.20) 0.19 (0.03, 1.12)
Intrathoracic liver 0.78 0.58
 No Reference Reference
 Yes 0.78 (0.13, 4.53) 1.60 (0.30, 8.57)
Hernia sac 0.78 0.94
 No Reference Reference
 Yes 1.77 (0.20, 15.51) 1.08 (0.16, 7.30)
ECMO 0.21 0.16*
 No Reference Reference
 Yes 0.32 (0.05, 1.89) 0.30 (0.05, 1.65)
Duration of ECMO support (d) 0.89 (0.64, 1.24) 0.49 0.99 (0.72, 1.36) 0.96
Oxygen requirement at 30 days of life 0.15* 0.03*
 No Reference Reference
 Yes 0.26 (0.04, 1.63) 0.13 (0.02, 0.85)
Oxygen requirement at discharge 0.02* 0.09*
 No Reference Reference
 Yes 0.10 (0.01, 0.74) 0.21 (0.04, 1.28)
Exclusively PO feeding at discharge 0.21 0.16*
 No Reference Reference
 Yes 3.16 (0.53, 18.84) 3.39 (0.61, 19.00)
Length of index hospitalization (d) 0.99 (0.97, 1.00) 0.12* 0.97 (0.95, 1.00) 0.07*
Re-hospitalization in the first 5 years of life 0.39 0.14*
 No Reference Reference
 Yes 0.46 (0.07, 2.80) 0.26 (0.04, 1.58)
Healthcare payer type 0.31 0.07*
 Public Reference Reference
 Private 2.47 (0.43, 14.33) 5.16 (0.89, 30.00)
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*

Variables with P ≤0.2 on bivariate analyses were included in multivariable logistic regression models.

Abbreviations: AGA, appropriate for gestational age (birth weight 10th - 90th percentile); CDH, congenital diaphragmatic hernia; CI, confidence interval; ECMO, extracorporeal membrane oxygenation; OR, odds ratio; PO, by mouth

In addition, CDH survivors who were discharged home on supplemental oxygen were 92% less likely to be proficient on the fourth grade literacy achievement test (OR=0.10; 95% CI 0.01-0.74; P=0.02). The AUC of the literacy model was estimated 0.77 (95% CI 0.57-0.98).

DISCUSSION

Our study compared fourth grade literacy and mathematics academic proficiency between surviving children who were born with CDH and attended public school in Arkansas and their unaffected controls. Our study also examined the impact of maternal and neonatal characteristics on the achievement test scores among children with CDH. Although the difference in the academic performance between CDH cases and controls did not reach statistical significance, CDH survivors were less proficient than controls on literacy and mathematics standardized tests. In addition, the need for oxygen at time of discharge, a longer hospital stay, and/or a public healthcare payer were predictive of worse academic performance among CDH survivors.

The clinical characteristics of our CDH cohort were consistent with the percentages of posterolateral and left-sided hernia defects previously reported in the literature (Dott et al., 2003; Deprest et al., 2014). However, 90% (38/42) of our CDH cases had an isolated CDH, a higher proportion than formerly reported (50-60%) (Dott et al., 2003). In addition, our CDH cohort was typically repaired within 72 hours of being placed on ECMO support, which is five days earlier compared to neonates reported in the Congenital Diaphragmatic Hernia Study Group (Dassinger et al., 2010).

A limited number of studies have previously compared ND outcomes at school age in CDH survivors versus controls with similar characteristics at birth. Mesas Burgos et al evaluated 326 CDH patients (≥15 years old) and 1577 controls and noted that a higher percentage of CDH survivors did not attain a school or university degree compared to their controls (17% vs. 10%, P=0.001). However, when evaluating CDH survivors who successfully achieved their school degree, the authors could not detect a significant difference between school achievements and highest educational level attained between cases and controls (Mesas Burgos et al., 2020). Frisk et al reported a higher frequency of clinically significant impairment on full-scale IQ measures among 15 CDH non-ECMO treated survivors (15.5%) versus 18 controls (0%) at a mean age of 13 years (Frisk et al., 2011). In contrast, Jakobson et al could not detect a significant difference on Full Scale IQ testing at 10-16 years of age between 13 CDH non-ECMO treated survivors and 11 controls, though CDH patients had more frequent evidence of visual-motor and oral-motor impairment (Jakobson et al., 2009). Although our findings were consistent with some prior reports, we uniquely examined the impact of childhood re-hospitalization and socioeconomic measures (payer type and maternal education) between CDH survivors and controls and compared their academic performance on fourth grade standardized testing, a measure more highly aligned with college attendance and adult economic productivity (Ritchie & Bates, 2013).

Several risk factors including prolonged oxygen supplementation, hospital length of stay >100 days, and public healthcare payer type, were previously identified in the literature and similarly noted in our analysis, to increase the risk of adverse ND outcomes among CDH patients (Antiel et al., 2017; D’Agostino et al., 1995; Danzer et al., 2010, 2017; Cortes et al., 2005; Sameroff, 1998; Stolar et al., 1995; Mesas Burgos et al., 2020). While ECMO and lower gestational age have also been associated with an increased risk of adverse ND outcomes (Madderom et al., 2013; Danzer et al., 2016), we did not detect an association between these variables and worse proficiency in either literacy or mathematics. These findings may have been affected by our limited sample size, or due to the majority of our surviving CDH cases being identified as 38 weeks gestational age or greater age at the time of delivery.

Our study had multiple strengths including the linkage of multiple large databases within a single state, the collection of detailed neonatal clinical variables, and the inclusion of socioeconomic measures. We also reported educational outcomes rather than psychometric testing. However, limitations remain. Although we acknowledge our sample size was small, our cohort is amongst the largest studies that evaluated school age educational outcomes of children with CDH versus unaffected controls (Jakobson et al., 2009; Frisk et al., 2011). Even though only 60% of our study cohort were linked to their educational data, the characteristics of the linked and unlinked CDH survivors were similar (Table 2). We also lacked data on detailed analgesic exposure, which could also impact ND outcomes. Nonetheless, our study provides clinicians and families with additional data regarding the school age academic performance of children with CDH.

CONCLUSION

As survival of infants born with CDH has continued to improve over the last decade, we need to better understand their educational outcomes and the impact of neonatal and maternal variables on their academic performance. Our study determined that CDH survivors were less proficient than controls on fourth grade literacy and mathematics achievement tests, although the difference between the two groups were not statistically significant. In addition, we identified three variables, the need for oxygen at time of discharge, a longer hospital stay, and/or a public healthcare payer, that were predictive of worse academic performance among these patients. Future studies should utilize multiple population databases to evaluate the educational outcomes among infants born with this rare congenital defect and examine the role of different factors on their academic performance in adolescence.

Supplementary Material

Supplemental.Table1

Acknowledgments:

The authors thank James Robbins, PhD Professor Emeritus, for his work as Principal Investigator of the original grant which established data linkages between health and education outcomes used in this study.

Funding Source:

March of Dimes (grant number 1U38OT000199 [to JR])

Abbreviations:

AOR

adjusted odds ratio

AUC

area under the curve

CDH

congenital diaphragmatic hernia

ECMO

extracorporeal membrane oxygenation

IQR

interquartile range

ND

neurodevelopmental

Footnotes

Prior Presentation: The abstract and the preliminary findings of this article were accepted for poster presentation at the Pediatric Academic Societies Meeting, May 2020.

Conflict of Interest: The authors have no financial relationships relevant to this article to disclose.

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Supplementary Materials

Supplemental.Table1
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