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Feasibility and Outcomes of Fetoscopic Tracheal Occlusion for Severe Left Diaphragmatic Hernia

Belfort, Michael A., MD, PhD; Olutoye, Oluyinka O., MD, PhD; Cass, Darrell L., MD; Olutoye, Olutoyin A., MD, MSc; Cassady, Christopher I., MD; Mehollin-Ray, Amy R., MD; Shamshirsaz, Alireza A., MD; Cruz, Stephanie M., MD; Lee, Timothy C., MD; Mann, David G., MD; Espinoza, Jimmy, MD; Welty, Stephen E., MD; Fernandes, Caraciolo J., MD; Ruano, Rodrigo, MD, PhD

doi: 10.1097/AOG.0000000000001749
Contents: Original Research
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OBJECTIVE: To evaluate feasibility and initial outcomes of fetoscopic tracheal occlusion for severe diaphragmatic hernia compared with a historical cohort who had not received fetal tracheal occlusion.

METHODS: Outcomes in a prospective observational cohort who underwent fetoscopic tracheal occlusion for severe fetal left diaphragmatic hernia without associated anomalies were compared with our historical nontreated cohort of matched fetuses of similar severity. Fetuses were classified using the same ultrasonography and magnetic resonance imaging methodology—prospectively in the fetoscopic tracheal occlusion group and retrospectively in the historical nontreated cohort. Obstetric and postnatal outcomes were evaluated and compared.

RESULTS: Between January 2004 and June 2015, 218 fetuses with diaphragmatic hernia were evaluated. Twenty (9%) fetuses had severe left diaphragmatic hernia (lung–head ratio 1.0 or less and liver herniation), of which 9 of 20 were managed without tracheal occlusion. Eleven were offered the procedure and in 10, it was successful. Mean (±standard deviation) gestational age was 27.9±1.1 weeks at attempted balloon placement, 34.1±1.1 weeks at removal, and 35.3±2.2 weeks at delivery. One patient required an ex utero intrapartum treatment procedure at delivery to remove the balloon. There were no maternal complications or fetal deaths. All neonates underwent postnatal repair with a patch. The 6-month, 1-year, and 2-year survival rates were significantly higher in our treated cohort than in our nontreated historical cohort (80% compared with 11%, risk difference 69%, 95% confidence interval [CI] 38–100%, P=.01; 70% compared with 11%, risk difference 59%, 95% CI 24–94%, P=.02; and 67% compared with 11%, risk difference 56%, 95% CI 19–93%, P=.04, respectively) with reduced need for extracorporeal membrane oxygenation (30% compared with 70%, risk difference 40%, 95% CI 10–79%, P=.05).

CONCLUSION: Fetoscopic tracheal occlusion is feasible and is associated with improved postnatal outcomes in severe left diaphragmatic hernia.

CLINICAL TRIAL REGISTRATION: ClinicalTrials.gov, https://clinicaltrials.gov, NCT00881660.

Fetoscopic tracheal occlusion is feasible and may improve lung growth and postnatal outcome in severe left diaphragmatic hernia.

Texas Children's Fetal Center and the Departments of Obstetrics and Gynecology, Surgery, Anesthesiology, and Radiology, and the Section of Neonatology, Department of Pediatrics, Baylor College of Medicine, Houston, Texas.

Corresponding author: Michael A. Belfort, MD, PhD, Texas Children's Hospital - Pavilion for Women, 6651 Main Street, Suite 1040F, Houston, TX 77030; email: belfort@bcm.edu.

Financial Disclosure The authors did not report any potential conflicts of interest.

Presented at the Society for Maternal-Fetal Medicine's 36th Annual Pregnancy Meeting, February 1–6, 2016, Atlanta, Georgia.

Each author has indicated that he or she has met the journal's requirements for authorship.

Congenital diaphragmatic hernia occurs sporadically in 1 of 3,000 live births and is usually diagnosed during the late second trimester.1,2 The diaphragmatic defect is left-sided in 85% of cases with 35% presenting with an associated major anomaly inclusive of aneuploidy.1 Despite advances in neonatal care, postnatal mortality remains high in neonates with severe congenital diaphragmatic hernia and is primarily related to pulmonary hypoplasia and pulmonary arterial hypertension.3

Fetoscopic tracheal occlusion is a procedure performed percutaneously with ultrasound-guided uterine access and fetoscopic deployment of a detachable tracheal balloon with the objective of promoting fetal lung growth.4,5 Fetoscopic tracheal occlusion has been proposed for fetuses with no associated major anomalies and severe congenital diaphragmatic hernia. Severe diaphragmatic hernia has been variably defined as a lung-to-head ratio less than 1.0, observed-to-expected lung-to-head ratio less than 0.25, or observed-to-expected total lung volume less than 0.35 and percentage of liver herniation greater than 21%.4–10 Recent trials in Europe and South America have suggested that fetuses with severe isolated diaphragmatic hernia have higher survival rates after fetoscopic tracheal occlusion than those patients treated only postnatally with or without the use of extracorporeal membrane oxygenation (60% compared with 5–20%, respectively).6,7,9–12

We report the initial outcomes of a fetoscopic tracheal occlusion program at our hospital. The main objectives of the present study were to report on the feasibility, safety, and outcomes of fetoscopic tracheal occlusion for severe left-sided diaphragmatic hernia. In addition, we aimed to compare the 6-month, 1-year, and 2-year survival rates of our treated fetuses with historical nontreated fetuses with severe left diaphragmatic hernia at our center.

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MATERIALS AND METHODS

A prospective cohort of patients treated with fetoscopic tracheal occlusion between March 2012 and June 2015 were compared with a historical control cohort of matched patients with severe diaphragmatic hernia treated without tracheal occlusion between January 2004 and February 2012. All patients were treated at Texas Children's Hospital Fetal Center using the same postnatal protocol. The present study was approved by the Baylor College of Medicine institutional review board (H-28021) and the U.S. Food and Drug Administration (FDA) and was registered at Clinicaltrials.gov (NCT00881660). Fetoscopic tracheal occlusion was offered to pregnant mothers with fetuses diagnosed with severe diaphragmatic hernia (lung-to-head ratio less than 1.0 respectively with liver herniated into the chest) between 22 0/7 weeks and 29 6/7 weeks of gestation. Other inclusion criteria were 1) singleton pregnancy, 2) fetal echocardiogram confirming no major cardiac anomaly, 3) normal fetal karyotype, 4) absence of maternal contraindications to abdominal–fetoscopic surgery or general anesthesia, and 5) no history of latex allergy. Patients who met criteria were counseled by a multidisciplinary team at Texas Children's Fetal Center and gave signed, written, informed consent. Eligible women were required to stay in close proximity to the hospital during the time interval between balloon placement and removal.

The surgery was performed under spinal anesthesia in our first four patients and subsequently with local anesthesia supplemented with intravenous sedation. Fetal anesthesia was given with a percutaneous ultrasound-directed intramuscular combination of fentanyl (15 micrograms per kilogram), atropine (20 micrograms per kilogram), and vecuronium (0.1 mg/kg). External cephalic version was performed as needed to appropriately position the fetus under ultrasound guidance and access to the fetal airway was planned taking into account placental location, fetal presentation, and attitude of the fetal head.

Under continuous ultrasound guidance (Video 1, available online at http://links.lww.com/AOG/A887), using a standard sterile technique, a 10-Fr Teflon cannula was inserted percutaneously into the amniotic cavity using an 18-G needle and the Seldinger technique. A 1.3-mm fetoscope was passed through the cannula into the amniotic fluid. With a combination of ultrasound guidance and direct endoscopic visualization, the endoscope was guided into the fetal larynx and through the vocal cords. Correct positioning was confirmed by verifying tracheal rings leading to the carina. A detachable latex balloon was placed in the fetal trachea halfway between the carina and the vocal cords. The balloon was inflated with sterile saline to a diameter of 2.2 mm for a length of 2 cm to occlude the fetal trachea. The endoscope and cannula were then removed. A Gelfoam plug was left in the cannula track as the port was removed. Mothers were given prophylactic antibiotics preoperatively (2 g cefazolin intravenously or 900 mg clindamycin intravenously) and treated with prophylactic tocolysis postoperatively (10 mg nifedipine every 4 hours orally or 25 mg indomethacin every 6 hours orally for a maximum of 2 days and then 10 mg nifedipine every 6 hours orally until 34 weeks of gestation as needed).

Video 1.

Video 1.

All patients had bedrest for 24 hours after fetoscopic tracheal occlusion. Once stable, mothers were discharged home on modified bedrest for 2 weeks (then unrestricted activity) and were required to stay within 30 minutes of the hospital to permit emergent balloon retrieval in the event of preterm labor or prelabor rupture of membranes. Mothers were seen once a week and the fetus was monitored at that visit for the duration of balloon occlusion. Fetal lung volumes were measured weekly and amniotic fluid volume and membrane status were monitored. Serial growth scans were performed every 3 weeks and a follow-up fetal magnetic resonance imaging (MRI) was performed 4–6 weeks postballoon occlusion.

Balloon retrieval was scheduled at 34 weeks of gestation, when the fetus would be an appropriate extracorporeal membrane oxygenation candidate if delivered prematurely. Previous data suggest improved neonatal outcomes with reversal of tracheal occlusion for several weeks before birth. The balloon was removed fetoscopically (using the same type of fetoscope as used for the balloon placement along with a grasping forceps) or, if necessary, was punctured under ultrasound guidance (using a 22-gauge needle). In the event of preterm labor with the balloon still in place, the balloon was to be removed from the fetal airway by direct bronchoscopy during an ex utero intrapartum treatment procedure. Maternal postoperative recovery after the balloon retrieval procedure was similar to that previously described for balloon placement.

All deliveries were planned to be vaginal unless an emergency ex utero intrapartum treatment was required or a cesarean delivery was obstetrically indicated. All neonates included in the present study were managed and treated at our facility according to a standardized diaphragmatic hernia treatment algorithm.13,14 Neonates were supported with extracorporeal membrane oxygenation in the presence of persistent hypoxia (preductal SaO2 less than 85%), persistent acidosis (pH less than 7.2), inadequate tissue perfusion despite maximal ventilatory support, or all of these and inotropic agents. Repair of the congenital diaphragmatic hernia was performed after the neonate was deemed to have achieved cardiorespiratory stability. Obstetric data from the 11 women who had fetoscopy were used in the analysis; neonatal data from only those 10 neonates who had successful fetoscopic tracheal occlusion were used.

The ultrasonography and MRI findings of all neonates in this study have been evaluated previously in a blinded fashion by an uninvolved researcher using the same equipment and techniques and the lung-to-head ratio, observed-to-expected lung-to-head ratio, observed-to-expected total fetal lung volumes, and percentage of liver herniation were calculated contemporaneously.15 The lung-to-head ratio was obtained using the longest axis method.15,16 In each case, the observed-to-expected lung-to-head ratio was calculated and expressed as a percentage.17 Total fetal lung volume was calculated on axial T2-weighted MRI using the method described by Mehollin-Ray et al18 and expressed as observed-to-expected total fetal lung volume by dividing the measured value by the mean expected fetal lung volume at the respective gestational age of each fetus.19 The percentage of liver herniation was measured using the technique described by Lazar et al.20 In addition, to confirm the severity of the cases, retrospectively the fetal stomach position was graded according to the method used by Cordier et al.21

We compared our 6-month tracheal occlusion survival rate with that of our matched historical cohort of consecutive patients in a control group (n=9) with left-sided diaphragmatic hernia of similar severity who did not undergo tracheal occlusion. All patients and those in the control group satisfied the same inclusion criteria (isolated left-sided congenital diaphragmatic hernia with lung-to-head ratio 1.0 or less and thoracic liver herniation) and were treated by the same team with access to extracorporeal membrane oxygenation.16 In addition, a further stratified analysis considering only fetuses with lung-to-head ratio less than 1.0, observed-to-expected total lung volume less than 0.35, and percentage liver herniation greater than 0.21 was performed.

The 1-year and 2-year survival rates in this cohort of patients were also evaluated, as well as the 2-year respiratory morbidity. Nonparametric testing was used including the Mann-Whitney U test and Kaplan-Meier and Cox regression for the survival analysis. P≤.05 denoted statistical significance.

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RESULTS

Between January 2004 and June 2015, 218 fetuses with diaphragmatic hernia were evaluated at Texas Children's Fetal Center. There were two cohorts: January 2004 to February 2012 (prefetal therapy) and March 2012 to June 2015 (fetoscopic tracheal occlusion group; Fig. 1). During the fetoscopic tracheal occlusion period, 11 of 80 patients (14%) satisfied the inclusion criteria for fetal treatment. All patients who satisfied criteria and who were offered the fetoscopic tracheal occlusion procedure accepted it. Of these, 10 of 11 (91%) had successful balloon placement (Table 1). In one neonate, fetoscopy was performed but a balloon could not be placed in the trachea and the procedure was abandoned. Nine patients in the historical cohort satisfied the same inclusion criteria and were used as a control group. The postnatal treatment of neonates in the case and control groups was similar and involved the same team of surgeons and neonatologists with access to extracorporeal membrane oxygenation.

Fig. 1.

Fig. 1.

Table 1.

Table 1.

Fetoscopic tracheal occlusion was attempted at a gestational age of 27.9±1.1 weeks. In six cases, the balloon was retrieved through a second fetoscopy at a mean gestational age of 34.5±0.3 weeks (Table 2). The gestational age at tracheal unblocking by any method (fetoscopy, ex utero intrapartum treatment, and needle puncture) was 34.1±1.1 weeks. The interval between balloon placement and fetoscopic removal was 6.1±1.4 weeks. In one patient with prelabor rupture of membranes and in one patient with chorioamnion separation, it was not possible to perform a repeat fetoscopy. These two fetuses underwent ultrasound-guided puncture of the balloon 3.0 and 5.1 weeks of gestation after fetoscopic tracheal occlusion. An ex utero intrapartum treatment procedure with balloon removal was performed in one fetus 6 weeks after fetoscopic tracheal occlusion as a result of preterm delivery. In one patient, the balloon was found to have been spontaneously expelled at the time of the fetoscopic procedure at 34 weeks of gestation. There were no cases of placental abruption, chorioamnionitis, maternal blood transfusion, maternal thrombosis, or fetal demise. Spontaneous preterm prelabor rupture of membranes (less than 37 weeks of gestation) occurred in 3 of 11 (27.3%) patients who had fetoscopy (31.5, 31.4, and 35.0 weeks of gestation) but in only 2 of 11 (18.1%) at less than 32 weeks of gestation (Table 3).

Table 2.

Table 2.

Table 3.

Table 3.

The mean gestational age at birth of the 11 patients was 35.3±2.2 weeks, with a median interval time between balloon removal and puncture and birth of 7 (0–35) days (Table 2). Four of the 11 patients (36.4%) had a vaginal delivery, and 7 of 11 (63.6%) had a cesarean delivery for obstetric indications (including a single ex utero intrapartum treatment procedure with balloon removal). The median Apgar score at 5 minutes was 7.2–4 The median umbilical arterial pH of the 10 fetoscopically treated neonates at delivery was 7.30 (7.26–7.35).

In the 10 patients in whom the balloon was successfully placed, there were significant increases in all indicators of lung volume despite no significant change in liver herniation (Fig. 2). Postnatal surgical repair of the diaphragmatic defect was performed in all patients on day 2–4 of life. All neonates had very large diaphragmatic defects requiring a patch.

Fig. 2.

Fig. 2.

Eight of 10 (80%) fetuses undergoing fetoscopic tracheal occlusion survived to 6 months. One child died at 17 days of life as a result of severe pulmonary hypertension, and another died at 4 months from pulmonary hypertension associated with pulmonary capillary hemangiomatosis, an unrelated but typically lethal condition. Another child died at 8 months from persistent pulmonary hypertension and progressive respiratory failure. Of the remaining seven children, six have been discharged alive, and, at the time of manuscript submission, one patient remains hospitalized (23 months); thus, survival rates to 1 year and 2 years of life were 70% (7/10) and 67% (6/9), respectively (Table 3). The median length of stay to discharge for survivors was 87 days (range 56–133 days). At 6 months, four of eight (50%) of the surviving infants required supplemental oxygen.

Tables 1 and 2 show prenatal fetal measurements and outcomes in our treated and nontreated treated cohorts using a lung-to-head ratio 1.0 or less and liver herniation. The 6-month, 1-year, and 2-year survival rates were statistically higher in the fetoscopic tracheal occlusion group (80% compared with 11%, risk difference 69%, 95% confidence interval [CI] 38–100%, P=.01; 70% compared with 11%, risk difference 59%, 95% CI 24–94%, P=.02; and 67% compared with 11%, risk difference 56%, 95% CI 19–93%, P=.04, respectively). Extracorporeal membrane oxygenation utilization was higher in the nontreated group (70% compared with 30%, risk difference 40%, 95% CI 10–79%, P=.05).

When we considered only the most severe of our fetoscopic tracheal occlusion group compared with nontreated patients (Table 3) using all accepted measures (ultrasonography: lung-to-head ratio less than 1.0 and observed-to-expected and lung-to-head ratio less than 0.25 and liver herniation and MRI: observed-to-expected and total fetal lung volume less than 0.32 and liver herniation greater than 0.21), the survival rates to 6 months, to discharge, to 1 year of life, and to 2 years of life were all significantly higher in the fetoscopic-treated group. Extracorporeal membrane oxygenation utilization was also higher in the nontreated group. Figure 3 shows a Kaplan-Meier analysis for the fetoscopic tracheal occlusion and nontreated groups (P<.01).

Fig. 3.

Fig. 3.

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DISCUSSION

Our study has demonstrated that, in an appropriately resourced U.S. setting, fetoscopic tracheal occlusion is feasible, safe, and may offer survival benefit in fetuses with severe isolated left-sided diaphragmatic hernia. These results are in agreement with a recent randomized controlled trial showing improved survival in the fetoscopically treated patients.10

The 6-month survival rate (80%) is higher when compared with a composite of comparable published outcomes on fetoscopic tracheal occlusion programs in European and South American centers (50%)5–7,10–12,21–25 and also higher than published series of similarly severe left diaphragmatic hernia managed without tracheal occlusion but with extracorporeal membrane oxygenation (20–50%).16,26–29

In our own center, our historical cases that would have met our inclusion criteria for fetoscopic tracheal occlusion had a lower 6-month survival when compared with our treated population (Table 2).16 In addition to improving the lung size and the 6-month survival rate, fetoscopic tracheal occlusion also reduced the need for extracorporeal membrane oxygenation in our unit (78–30%). These differences in survival and need for extracorporeal membrane oxygenation are even more pronounced if all prenatal measures of severity are used for inclusion (ultrasonography and magnetic resonance imaging; Table 3). Reducing the need for extracorporeal membrane oxygenation in these patients has important clinical and economic implications given the risks of this therapy (especially cerebral hemorrhage).

Safety was of primary interest in the design and implementation of this study. Measures were put in place to facilitate emergency balloon retrieval and to minimize any risk of airway obstruction at birth in fetuses with a balloon in place. A specialized team was on call 24/7 during the time the balloon was in place; training of this team included simulation of emergency balloon removal with a life-like model30 for all involved health care providers. Our system was tested in one patient in which ex utero intrapartum treatment was required because of rapidly progressive preterm labor and it functioned as planned.

This study was conducted under special oversight by the FDA under stringent conditions. During our study, the Goldvalve balloon, which was FDA-approved for neurosurgical use, was discontinued, precluding our off-label use for fetoscopic tracheal occlusion. The FDA office assisted in obtaining an Investigational Device Exemption for the Balt balloon, which is not FDA-approved.

Limitations of our study include a nonrandomized study design, small sample size, and the fact that these results represent a single center with a team that had prior fetoscopic tracheal occlusion experience. One particular issue that must be addressed is the potential for confounding as a result of changes in management over the 8 years during which patients in the control group were treated. Although this is a valid concern, in terms of neonatal intensive care unit protocols, use of ventilation and drug (ie, nitric oxide) strategies, extracorporeal membrane oxygenation availability, surgeons and surgical technique, and postdelivery management, there has been minimal change with the same team of surgeons managing all patients with diaphragmatic hernia since 2001.

In conclusion, our results suggest that fetoscopic tracheal occlusion may be a useful adjunctive prenatal therapy to improve the outcomes of fetuses with severe and extremely severe left- sided diaphragmatic hernia in a U.S.-based health care system with extracorporeal membrane oxygenation capability.

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