PEDIATRICS Vol. 110 No. 3 September 2002, pp. 590-596
Survival in Early- and Late-Term Infants With Congenital Diaphragmatic Hernia Treated With Extracorporeal Membrane Oxygenation
* Division of Neonatology
Division of General Pediatrics, Department of Pediatrics, Strong Children’s Research Center, Golisano Children’s Hospital at Strong
Department of Community and Preventive Medicine, University of Rochester Medical Center, Rochester, New York
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONREFERENCES |
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Background. Congenital diaphragmatic hernia (CDH) is a malformation of the diaphragm that allows bowel to enter the thoracic cavity, resulting in pulmonary hypoplasia and pulmonary hypertension. Approximately 50% of CDH patients are treated with extracorporeal membrane oxygenation (ECMO). The optimal gestational age for delivery of term infants with CDH at high risk for requiring ECMO is not known. The goal of this study was to compare survival of infants with CDH receiving ECMO born early term (38 0/7–39 6/7 weeks’ gestation) with those born late term (40 0/7–41 6/7 weeks’ gestation). Changes in survival rates of term infants and the factors associated with these changes were assessed over the 25 years that ECMO has been available.
Methods. Design. Retrospective cohort study of infants with CDH treated with ECMO.
Data Sources. The Extracorporeal Life Support Organization registry of patients treated at active Extracorporeal Life Support Organization centers from April 1976 through June 2001.
Analysis. Survival and clinical predictors of survival were compared between infants born early term (38 0/7–39 6/7 weeks’ gestation) and infants born late term (40 0/7–41 6/7 weeks’ gestation). Changes in survival rates over time and factors associated with survival were evaluated.
Results. Among full-term infants with CDH treated with ECMO, late-term compared with early-term delivery was associated with improved survival (63% vs 53%). Among full-term survivors of ECMO, late-term infants spent less time on ECMO (181 vs 197 hours) and less time in the hospital (60 vs 67 days). In multivariate analysis, greater birth weight, higher 5-minute Apgar score, higher arterial pH and PCO2 <50 torr before ECMO, and absence of a prenatal diagnosis of CDH were associated with survival.
Since the late 1980s, survival of infants with CDH requiring ECMO decreased from 63% to 52%. The decreased survival rate was associated with increased rates of prenatal diagnosis, early-term delivery, lower birth weight, longer ECMO runs, and more frequent complications on ECMO.
Conclusions. Among term infants with CDH receiving ECMO, late-term delivery compared with early-term delivery is associated with improved survival, shorter ECMO duration, shorter hospital length of stay, and fewer complications on ECMO. These data suggest that, at least for the 
50% of CDH patients treated with ECMO, outcomes for infants with CDH may be improved by delay of elective delivery until 40 completed weeks of gestation.
Key Words: congenital diaphragmatic hernia • extracorporeal membrane oxygenation • survival • gestational age • Extracorporeal Life Support Organization Registry
Abbreviations: CDH, congenital diaphragmatic hernia • iNO, inhaled nitric oxide • ECMO, extracorporeal membrane oxygenation • ELSO, Extracorporeal Life Support Organization • LOS, length of stay • OR, odds ratio
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONREFERENCES |
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Congenital diaphragmatic hernia (CDH), which occurs in 1 in 3000 to 4000 deliveries, is a long-recognized cause of newborn morbidity and mortality.1 In 1848, Vincent Bochdalek, a Prague anatomist, first described CDH occurring through a posterolateral defect in the diaphragm. One hundred years after the first successful surgical repair of CDH in an infant in 1902, the mortality rate for infants with CDH remains high (31%–58%).2–6 Newer therapies, such as high-frequency oscillatory ventilation, gentle ventilation strategies, inhaled nitric oxide (iNO), and a variety of antenatal and postnatal surgical approaches, have not eliminated the need for extracorporeal membrane oxygenation (ECMO) as a rescue therapy.5,7–15 In the Neonatal Inhaled Nitric Oxide Study Group randomized trial of iNO in infants with CDH, ECMO was used in 54% of control and 80% of iNO-treated infants.11 In another study of 461 infants with CDH, ECMO was used in 54% of patients.5
Preterm delivery and low birth weight are risk factors for mortality on ECMO, whereas postdates delivery is a risk factor for pulmonary hypertension, a common complication of CDH.8,9 In attempt to balance these risks, some clinicians advocate early-term delivery (38 weeks’ gestation); however, the optimal gestational age for delivery of infants with CDH is not known.16,17 Of the 8% to 25% of infants who die before receiving ECMO, many infants have such severe pulmonary hypoplasia, pulmonary hypertension, or associated congenital anomalies that they cannot be stabilized or are not considered ECMO candidates.15, 18 Infants with CDH who are treated with ECMO represent a subgroup of infants for whom mortality is considered potentially preventable. Understanding clinical characteristics leading to improved ECMO survival will contribute to improved overall survival of infants with CDH. The purpose of this study was to determine gestational age-specific survival rates within the range of term gestation for infants with CDH requiring ECMO. We also assessed changes in survival rates over the 25 years that ECMO has been available and examined potential predictors of these changes.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONREFERENCES |
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Data Source and Definitions
Data from the Extracorporeal Life Support Organization (ELSO) Registry for all infants with CDH treated with ECMO born April 1976 through June 2001 were obtained in an electronic database. ELSO is an international consortium of 115 ECMO centers in which participation and data reporting are voluntary. It is not a population-based source of data for clinical disorders; only ECMO-treated infants are enrolled. Clinical observations were categorized as pre-ECMO (collected immediately before initiating ECMO) and post-ECMO (collected after initiation of ECMO; Table 1). Hospital length of stay (LOS) was defined as the difference (days) between birth and discharge dates. Gestational age was determined by obstetric dating. Analysis did not require informed consent by the University of Rochester Institutional Review Board.
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Strategy of Analysis
Determination of Gestational Age-Specific Outcomes
Variation in survival, hospital LOS and duration of ECMO by gestational age was determined. Data from infants born within 2 weeks of their mother’s estimated date of confinement (38 0/7–41 6/7 weeks’ gestation) were subjected to additional analysis. Multivariate analysis was performed for this term group, examining demographic and pre-ECMO parameters to identify independent predictors of survival among clinical data that would be available before initiating ECMO for an individual patient. To identify all independent predictors of survival including data regarding the clinical ECMO course, logistic regression analysis was repeated using demographic, pre-ECMO as well as post-ECMO data.
Evaluation of Variation in Survival Over Time
Four eras of ECMO therapy were defined before analysis as follows: Era 1, April 1976–1985; Era 2, 1986–1990; Era 3, 1991–1995; Era 4, 1996-June 2001. Era 1 includes the first patient with CDH treated with ECMO in the ELSO database and spans 9 years during which few CDH infants (n = 55) were treated with ECMO. The remaining time interval, 1986-June 2001, was divided into 3 time periods. Trends in survival, patient population and clinical course of infants with CDH receiving ECMO were analyzed.
Statistics
Data were analyzed using SAS statistical software (SAS System, Cary, NC). Data fields were screened for obviously erroneous entries and missing data points. Six records lacked gestational age and were excluded from the analysis. Bivariate analysis was performed using the 
2 test for categorical variables and t test or analysis of variance for unequal sample sizes for continuous variables. Results were considered significant at P < .05 2-sided. Analysis of variation in rates over time was performed using the Cochran Armitage test for trend. Logistic regression was performed using stepwise selection of independent variables (P entry = .05). Birth weight (kg), arterial pH (tenths), Apgar score, ECMO duration (days), and year of birth were analyzed as continuous variables; other variables were dichotomous. Logistic regression results are presented as odds ratios (OR), providing the relative odds of survival.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONREFERENCES |
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Gestational Age-Specific Outcomes
Between April 1976 and June 2001, 3460 infants >34 weeks’ gestation with CDH underwent ECMO. Of the 2406 infants born at 38 0/7 to 41 6/7 weeks’ gestation (69.5%), 1177 were born early term and 1229 were born late term (Table 2). More males than females with CDH received ECMO (57% vs 43%; P <.0001). Late- term infants were heavier, more likely to be delivered by elective cesarean section, less likely to have been diagnosed prenatally, and were younger at initiation of ECMO (Table 2). Survival increased with increasing gestational age from 33% for infants 34 to 35 6/7 weeks’ to 70% for infants >42 weeks’ gestation (P < .0001; Fig 1). The relative survival rate for late-term infants was nearly 20% greater than that for early-term infants (63% vs 53%, P < .0001; Fig 1). Early-term infants surviving ECMO spent an average of 16 hours longer on ECMO (P < .0001) and 7 days longer in the hospital than late-term infants (P < .0001; Fig 2).
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Multivariate analysis was performed on 2165 (90%) of the 2406 infants born 38 0/7 to 41 6/7 weeks’ gestation for whom demographic and pre-ECMO data were recorded in the ELSO record. Greater birth weight, absence of a prenatal diagnosis, higher 5-minute Apgar score, pCO2
50 torr at initiation of ECMO, higher arterial pH before ECMO, and earlier year of birth were independent predictors of survival (Fig 3A). Gestational age did not independently predict survival, but was correlated with birth weight (R = 0.3; P < .0001), which was associated with improved survival (OR: 2.5; confidence interval: 1.9–3.0). For full-term infants 38 0/7 to 41 6/7 weeks’ gestation, survival increased more than twofold from 35% at 2000 to 2499 g to 75% for infants 4000 to 4449 g (P < .0001; Fig 4).
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Variation in Survival Rates Over Time
After Era 1, survival for full-term infants fell from 63% in Era 2 to 52% in Era 4 (P < .0001; Fig 5). Over the same time period, survival for early-term infants fell from 61% to 48% (P < .01). Among late-term infants, a smaller decline in survival occurred (65% to 58%; P = .053). Factors associated with the fall in survival rates over time were determined by logistic regression. The model included 1842 (76%) of 2406 total infants for whom complete demographic, pre-ECMO, and post-ECMO data were available (Fig 3B). In this model, clinical parameters describing the ECMO course and complications replaced year of birth as an independent predictor of survival, suggesting that changes in the clinical ECMO course and complication rate account for a significant amount of the reduction in survival over time.
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Variation in Patient Characteristics Over Time
Patient data significantly associated with survival in multivariate analysis were analyzed by era to identify trends in the characteristics of ECMO treated infants over time (Table 3). The percentage of infants born early-term increased (40% in Era 1 to 57% in Era 4, P < .0001) and likely accounts for the decrease in average birth weight of term infants with CDH treated with ECMO. Prenatal diagnosis of CDH increased over 25 years from 4% in Era 1 to 51% in the most recent era. Within each era, infants born early-term had a higher prenatal diagnosis rate than infants born late term. In Era 4, the prenatal diagnosis rate among early-term infants was nearly twice as high as that for late-term infants (62% vs 36%; P < .0001). The survival rate for term infants diagnosed prenatally with CDH did not change appreciably over time. For infants not diagnosed prenatally, the survival rate decreased, most notably between Eras 3 and 4 (65% vs 53%). In the most recent era, both prenatally and postnatally diagnosed infants with CDH had a higher survival rate on ECMO than did early-term infants (58% vs 48%, P < .05, and 57% vs 48%, P = .05, respectively). These data show a temporal relationship between higher rates of prenatal diagnosis, early-term birth, lower birth weight, and decreased survival in term infants with CDH receiving ECMO.
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The percentage of infants on ECMO >7 days and with >4 complications on ECMO increased sharply over the 4 eras (Table 3). Among both early- and late-term infants, the frequency of renal, neurologic, and hemorrhagic complications decreased over time. However, in the most recent era, early-term infants were more likely to suffer a renal, neurologic, and hemorrhagic complication than were late-term infants (50% vs 40%; P < .01). Infants with these complications are presented in aggregate but show similar trends when analyzed individually.
Among respiratory severity parameters, the percentages of infants with peak inspiratory pressure 
40 cm H2O and with PaO2/FIO2 <0.4 at initiation of ECMO decreased over the 4 eras (Table 3). There was no significant difference in the incidence of low arterial pH (defined here as pre-ECMO arterial pH <7.2) or proportion of infants with pCO2 <50 torr between early- and late-term infants over the 4 eras. These patterns in respiratory severity before initiation of ECMO do not suggest that infants receiving ECMO in recent eras had greater respiratory compromise at initiation of ECMO.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONREFERENCES |
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Outcomes for Term Infants
In this survival analysis of term infants with CDH requiring ECMO, late-term infants (40–41 6/7 weeks’ gestation) compared with infants born early term (38–39 6/7 weeks’ gestation) had a 20% greater relative survival (63% vs 53%; P < .001), spent less time on ECMO, and spent less time in the hospital. Most recently, over the period January 1, 1996, to June 30, 2001, fewer late-term infants than early-term infants had 4 or more complications on ECMO or renal, neurologic, or hemorrhagic complications on ECMO— complications that were associated with mortality in multivariate analysis.
The cause of reduced survival of early-term infants with CDH on ECMO is not known. In multivariate analysis, greater birth weight was an independent predictor of survival, whereas gestational age was not. Hence, differences in survival between early- and late-term infants in this study are more strongly associated with birth weight than gestational age. A direct relationship between birth weight and greater survival for infants of all gestational ages with CDH treated with ECMO has been reported.8 Our study focuses the relationship between survival and greater birth weight to infants within the range of term gestation. In this study, late-term infants were nearly 10% heavier than early-term infants (3328 vs 3071 g; P < .0001). Because gestational age defines term gestation, can more readily be used as a criterion for elective term delivery, and is correlated with birth weight (R = 0.3; P < .0001), we chose to discuss survival rates by gestational age rather than by birth weight.
Variation in Survival Rates Over Time
Survival of term infants with CDH on ECMO decreased over the past 15 years (Eras 2–4, Fig 5) in both late-term and early-term infants. During this time, the percentage of CDH infants treated with ECMO that were delivered early term increased significantly, from 38% in Era 2 (1985–1990) to 57% in the most recent era (P < .001). We examined 3 potential explanations for the decrease in ECMO survival of term infants over the last 15 years. New therapies such as high-frequency oscillatory ventilation, iNO, gentler ventilation, and improved surgical approaches may have led to better survival without ECMO and resulted in sicker or less treatable infants coming to ECMO. To assess this, we evaluated clinical measures of pre-ECMO respiratory severity over time. There was no change in the average pH or incidence of low pH (<7.2) or median Apgar score at 5 minutes over the 4 eras. Pre-ECMO oxygenation of infants measured by PaO2/FIO2 ratio <0.4 improved throughout all 4 eras (a higher PaO2/FIO2 ratio reflects better oxygenation) and agrees with data from another study.19 Trends in pre-ECMO respiratory severity do not readily explain decreased survival rates observed in recent eras.
Changes in the duration of ECMO and the frequency and types of complications on ECMO were evaluated to determine their contribution to decreased survival in recent eras. The proportion of infants undergoing ECMO for >7 days increased from 22% to 66% (P <.001) over the 4 eras. Concurrent with longer ECMO runs was an increase in the number of infants with >4 complications on ECMO. In the most recent era, infants born early term were significantly more likely to have 4 or more ECMO complications and to have either a renal, neurologic, or hemorrhagic complication. Because greater birth weight has a protective effect against complications on ECMO, the trend toward earlier delivery at lower birth weight in the most recent eras may contribute to higher ECMO complication rates. Although a higher ECMO complication rate may reflect reporting bias toward more complete documentation, longer ECMO courses in recent eras are a likely reason for the observed increase in number of complications on ECMO.
Concurrent with the increase in number of early-term infants receiving ECMO, prenatal diagnosis of CDH has increased dramatically, especially for early-term infants (10% in Era 2% vs 51% in Era 4). During the most recent era, Era 4, early-term infants treated with ECMO were nearly twice as likely to have been diagnosed prenatally than were late-term infants (62% vs 36%; P < .0001). Prenatal diagnosis of CDH was associated with reduced ECMO survival (52% vs 61%; P < .0001). Several potential explanations exist. Recent reports found prenatal ultrasound to have up to a 55% false-negative rate in detecting CDH antenatally.20,22 Some authors suggest that the ability to diagnose CDH prenatally infers a larger diaphragmatic defect with more displaced bowel, greater pulmonary hypoplasia, and less treatable lung disease.20,21 Others, suggest that covariates with prenatal diagnosis, such as polyhydramnios, a poor prognostic factor for infants with CDH, may contribute to early-term delivery and reduced survival.23 Whether the increasing prenatal diagnosis rate resulted in more infants with CDH being delivered at early term and consequently to increased use of ECMO for early-term infants is not clear. Additional study is necessary to clarify the relationship between prenatal diagnosis and early-term delivery. However, in the most recent era, early-term infants with CDH treated with ECMO, whether diagnosed prenatally or postnatally, were less likely to survive than late-term infants (prenatal diagnosis, 48% vs 58%, P < .05 and postnatal diagnosis, 48% vs 57%, P = .052, early vs late term, respectively).
We wished to explore the possibility that increased prenatal diagnosis rates were associated with an increased rate of elective early-term delivery by either cesarean section or induced vaginal delivery. However, data from the ELSO include elective cesarean section but does not subdivide vaginal deliveries by cause of labor, induced versus spontaneous. Hence, the frequency of elective cesarean section underreports the overall frequency of elective delivery. We found no difference in survival between delivery by elective cesarean section and delivery following labor by cesarean section or the vaginal route. Although early-term infants were less likely than late-term infants to undergo elective cesarean section (26% vs 32%; P = .02), 26% of early-term infants were delivered by elective cesarean section without labor, suggesting that medical personnel and the infant’s family set the timing of delivery. Prenatal diagnosis was associated with early-term elective cesarean section delivery raising the possibility that prenatal diagnosis prompted a decision for earlier delivery, by either the elective cesarean section or induced vaginal route. Additional study is needed to determine the role of increasing numbers of early-term infants on the decrease in ECMO survival over the past 15 years.
Limitations
This study is limited by use of data exclusively from infants with CDH who required ECMO. It is possible that non-ECMO therapy is more effective in treating early-term infants with CDH than in treating late-term infants, thus offsetting poorer survival of early-term infants on ECMO. However, this is unlikely. ECMO is used as rescue therapy in 50% of CDH infants for whom mortality is high, but potentially preventable. Higher ECMO survival rates should contribute to higher overall survival of infants with CDH. Additional insight into differences in overall survival and changes in survival rates over time might be gained by a population-based study that includes postnatal survival for both ECMO and non-ECMO treated infants.
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CONCLUSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONREFERENCES |
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Infants born early term with CDH treated with ECMO have decreased survival, longer and more complicated ECMO courses, and longer hospital stays than infants born late term. Despite higher mortality for early-term infants than late-term infants, a growing number of infants receiving ECMO are born early term. Recent trends toward increased prenatal diagnosis rates of CDH may be responsible for higher numbers of early-term births at lower birth weight and at substantially higher risk to do poorly on ECMO. The data presented here provide evidence that, at least for the
50% of infants with CDH that are treated with ECMO, clinical outcomes may be improved by delay of elective delivery of infants with suspected CDH until 40 completed weeks’ gestation.
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FOOTNOTES |
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Received for publication Dec 10, 2002; Accepted Apr 17, 2002.
Address correspondence to Timothy P. Stevens, MD, Department of Pediatrics, Division of Neonatology, Golisano Children’s Hospital at Strong, Box 651, 601 Elmwood Ave, Rochester, NY 14642. E-mail:timothy_stevens{at}urmc.rochester.edu
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PEDIATRICS (ISSN 1098-4275). ©2002 by the American Academy of Pediatrics
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