Original Article
A Randomized Trial of Fetal Endoscopic Tracheal Occlusion for Severe Fetal Congenital Diaphragmatic Hernia
N Engl J Med 2003; 349:1916-1924November 13, 2003
- Abstract
Background
Experimental and clinical data suggest that fetal endoscopic tracheal occlusion to induce lung growth may improve the outcome of severe congenital diaphragmatic hernia. We performed a randomized, controlled trial comparing fetal tracheal occlusion with standard postnatal care.
Methods
Women carrying fetuses that were between 22 and 27 weeks of gestation and that had severe, left-sided congenital diaphragmatic hernia (liver herniation and a lung-to-head ratio below 1.4), with no other detectable anomalies, were randomly assigned to fetal endoscopic tracheal occlusion or standard care. The primary outcome was survival at the age of 90 days; the secondary outcomes were measures of maternal and neonatal morbidity.
Results
Of 28 women who met the entry criteria, 24 agreed to randomization. Enrollment was stopped after 24 patients had been enrolled because of the unexpectedly high survival rate with standard care and the conclusion of the data safety monitoring board that further recruitment would not result in significant differences between the groups. Eight of 11 fetuses (73 percent) in the tracheal-occlusion group and 10 of 13 (77 percent) in the group that received standard care survived to 90 days of age (P=1.00). The severity of the congenital diaphragmatic hernia at randomization, as measured by the lung-to-head ratio, was inversely related to survival in both groups. Premature rupture of the membranes and preterm delivery were more common in the group receiving the intervention than in the group receiving standard care (mean [±SD] gestational age at delivery, 30.8±2.0 weeks vs. 37.0±1.5 weeks; P<0.001). The rates of neonatal morbidity did not differ between the groups.
Conclusions
Tracheal occlusion did not improve survival or morbidity rates in this cohort of fetuses with congenital diaphragmatic hernia.
Media in This Article
Figure 1
Kaplan–Meier Survival Curves for the Study Group as of November 1, 2002 (3.5 Years after Study Initiation).Table 1
Base-Line Characteristics According to the Actual Treatment.Article Activity
- Article
Congenital diaphragmatic hernia can now be accurately diagnosed by mid-gestation, and the outcome in individual cases can be predicted on the basis of sonographic measurement of the lung-to-head ratio and the presence or absence of liver herniation into the thorax.1-4 Mortality is low for full-term fetuses without liver herniation and a favorable lung-to-head ratio (above 1.4) at tertiary centers.4 However, fetuses with liver herniation and a low lung-to-head ratio have high rates of mortality and morbidity, despite recent advances in intensive neonatal care, including extracorporeal membrane oxygenation, nitric oxide inhalation, high-frequency ventilation, and delayed operative repair of the diaphragmatic hernia.5-11
The fundamental problem in babies born with a congenital diaphragmatic hernia is pulmonary hypoplasia. A number of strategies have been used in an attempt to improve the growth of hypoplastic lungs before they are needed for gas exchange at birth. Anatomical repair of the hernia through open hysterotomy proved feasible, but it did not decrease mortality and was abandoned.12-19 Fetal tracheal occlusion was developed as an alternative strategy to promote fetal lung growth by preventing normal egress of lung fluid. Occlusion of the fetal trachea was shown to stimulate fetal lung growth in a variety of animal models.20-27 Techniques to achieve reversible fetal tracheal occlusion were explored in animal models28,29 and then applied clinically, evolving from the use of external metal clips placed on the trachea by means of open hysterotomy or fetoscopic neck dissection30-33 to internal tracheal occlusion with a detachable silicone balloon placed with the use of fetal bronchoscopy through a single 5-mm uterine port.34
Our initial experience suggested that fetal endoscopic tracheal occlusion improved survival in human fetuses with severe congenital diaphragmatic hernia.33,34 To evaluate this novel therapy, we conducted a randomized, controlled trial from April 1999 through July 2001 in which we compared tracheal occlusion with standard care; all women referred after April 1999 who were carrying fetuses with severe left-sided congenital diaphragmatic hernia and who met the inclusion criteria were invited to participate.
Methods
Referral and Evaluation
Women carrying fetuses with left-sided congenital diaphragmatic hernia and a normal karyotype underwent evaluation at the University of California, San Francisco, when the fetuses were 22 to 27 weeks of gestational age, including ultrasonography, calculation of the lung-to-head ratio, echocardiography, obstetrical consultation, and psychosocial assessment.
The eligibility criteria were the presence of left-sided congenital diaphragmatic hernia, a normal fetal echocardiogram, no ultrasonographic evidence of other anomalies, a normal karyotype, liver herniation into the left hemithorax, a lung-to-head ratio below 1.4 as measured between 22 and 28 weeks of gestation, a fetal age between 22 and 28 weeks of gestation, a singleton pregnancy, no preterm labor, and no medical contraindication to general anesthesia or psychosocial contraindication to participation by the mother. Families who met the eligibility criteria were extensively counseled, and those who wished to participate provided written, informed consent for both randomization and treatment. No fetal intervention was offered outside the trial. The committee on human research of the University of California, San Francisco, approved the trial protocol.
Block Randomization
Because lung-to-head ratio is the most accurate predictor of survival for fetuses with isolated left congenital diaphragmatic hernia and a herniated liver,1,3 randomization was performed with the use of permuted blocks stratified according to the lung-to-head ratio. Three strata of lung-to-head ratios were used: 0.78 or less, 0.79 to 1.06, and 1.07 to 1.39.
Fetal Endoscopic Tracheal Occlusion and Prenatal Care
The technique of fetal endoscopic tracheal occlusion has been described previously.29 Betamethasone was given to the mother preoperatively to improve fetal lung compliance.35 With the mother and fetus under general anesthesia and using a low transverse maternal laparotomy, we passed a 4-mm perfusion hysteroscope through a 5-mm trocar and guided it through the fetal vocal cords with the aid of both fetoscopic and cross-sectional ultrasonographic visualization. A detachable silicone balloon (Target Therapeutics) was placed in the fetal trachea midway between the carina and the vocal cords. The balloon was inflated with isosmotic contrast material so that it filled the fetal trachea (diameter, 0.5 mm) for a length of at least 2 cm. Experimental studies have shown that this maneuver effectively occludes the fetal trachea.34,36 The first two patients in this study underwent a three-port fetal endoscopic tracheal clip procedure,30 which was then replaced by the balloon-occlusion technique; the data safety monitoring board approved the change.
The women in the intervention group were treated with a preoperative indomethacin suppository (50 mg), intraoperative halogenated anesthetic agents with small doses of nitroglycerin as needed, postoperative magnesium sulfate and indomethacin (for a maximum of two days), and an oral calcium-channel blocker (nifedipine) until delivery. Beta-adrenergic agonists, which reduce the production of fetal lung fluids in animals,37,38 were used sparingly. The mothers were discharged to the nearby Ronald McDonald House of San Francisco, where they rested in bed and underwent ultrasonography and nonstress testing every other week until delivery.
All fetuses with tracheal occlusion were delivered by the EXIT (ex utero intrapartum therapy) procedure, as previously described.39 Briefly, the fetal head was delivered and bronchoscopy was performed through a low transverse cesarean hysterotomy. The balloon occluding the trachea was deflated and removed, the airway was suctioned, an endotracheal tube was inserted, an exogenous surfactant (Exosurf Neonatal, Glaxo Wellcome) was administered at a dose of 3 ml per kilogram of body weight, and assisted ventilation was begun before the umbilical cord was divided.
The women assigned to standard care were treated expectantly, with a planned return to the University of California, San Francisco, at 36 weeks of gestation. Antenatal steroids were administered if there was preterm labor (one case) or if the lung profile indicated immaturity (seven cases). If spontaneous labor did not occur, labor was induced. Delivery was vaginal unless cesarean section was indicated.
Neonatal Resuscitation and Respiratory Care
All infants in both groups underwent intubation immediately at birth and received pancuronium and sedatives as soon as vascular access was obtained (within five minutes in all cases). Conventional mechanical ventilation was performed to maintain the partial pressure of arterial carbon dioxide in the range of 45 to 60 mm Hg (permissive hypercapnia) and right-hand (preductal) oxygen saturation above 90 percent. Higher values for the partial pressure of arterial carbon dioxide and lower oxygen-saturation values were tolerated in the first hours of life. If ventilation and oxygenation were inadequate, high-frequency oscillatory ventilation, inhaled nitric oxide, and extracorporeal membrane oxygenation were used as needed. The diaphragmatic hernia was repaired when the infant's respiratory status had stabilized. The infants remained paralyzed and sedated from birth until 24 hours after operative repair. Once they had been weaned from ventilatory support, the infants continued to receive supplemental oxygen until the oxygen saturation was maintained at a level above 95 percent while they were breathing ambient air.
Outcome Analysis
The primary outcome was survival to the age of 90 days. Additional outcomes were short-term measures of neonatal pulmonary morbidity, including the need for extracorporeal membrane oxygenation and the duration of neonatal ventilatory support and administration of supplemental oxygen; gastrointestinal morbidity; neurologic morbidity; survival to discharge from the hospital; the duration of hospitalization; and maternal physical and psychological morbidity. Assessments of other measures of long-term morbidity (including the need for supplemental oxygen, rates of recurrent infection and repeated hospitalization, and neurodevelopmental outcomes) are ongoing and are not included here.
On the basis of a logistic-regression model derived from our historical data (57 cases of left-sided congenital diaphragmatic hernia, a lung-to-head ratio under 1.4, and liver herniation), a survival rate of 37 percent was predicted in the group receiving standard care. We calculated that a sample size of 40 subjects would provide the study with 80 percent power to detect an increase in the survival rate to 77 percent in the group undergoing fetal tracheal occlusion, at an alpha level of 0.05, with allowance for an interim review of the data.
We analyzed the data with the use of Student's t-test, the Mann–Whitney rank-sum test, the chi-square test, Fisher's exact test, logistic regression, and survival analysis (based on Cox proportional-hazards models). The results are reported as means ±SD and hazard ratios with 95 percent confidence intervals. A P value of less than 0.05 was considered to indicate statistical significance. The study was monitored by a data safety monitoring board appointed by the National Institutes of Health (NIH) (see the Appendix).
Results
Early Termination of the Trial
Enrollment was terminated early, in August 2001, after 24 patients had been randomly assigned to treatment groups, on the recommendation of the data safety monitoring board. This recommendation was based on a conditional probability calculation that predicted a failure to detect a difference in survival to 90 days of age with the planned enrollment; this interim analysis was performed when data on 18 subjects were available for review of the primary outcome 27 months after enrollment had begun.
Characteristics of the Study Subjects
A total of 157 women were referred by telephone, and 57 of them came to San Francisco for evaluation. Twenty-nine did not meet the criteria for enrollment (because of associated anomalies in 11, a diaphragmatic hernia that did not meet the criteria for severity in 12, and psychosocial factors in 6). Twenty-four of the 28 eligible women agreed to randomization.
The majority of the enrolled women had fetuses that were in the middle stratum of lung-to-head ratio (0.79 to 1.06). Eleven women were initially randomly assigned to receive standard care (mean lung-to-head ratio, 0.96±0.20), and 13 were randomly assigned to undergo fetal tracheal occlusion (mean lung-to-head ratio, 0.97±0.14). Two of the women randomly assigned to undergo fetal tracheal occlusion opted to have standard care, so that 13 women received standard care (lung-to-head, ratio 0.96±0.20), and 11 underwent fetal tracheal occlusion (lung-to-head ratio, 0.97±0.14). The base-line characteristics of the two groups according to the actual treatment received are shown in Table 1Table 1
Base-Line Characteristics According to the Actual Treatment.. The lung-to-head ratio did not differ significantly between the groups, whether the data were analyzed on an intention-to-treat basis (P=0.82) or according to the actual treatment (P=0.52), nor were there significant differences in any other base-line characteristics, whether they were compared on the basis of the assigned treatment or the actual treatment. The duration of tracheal occlusion was 36.2±14.7 days, with a range of 16 to 64 days.Pregnancy Outcomes and Complications
As expected, there was substantial short-term maternal morbidity after the fetal intervention. All women in the tracheal-occlusion group required tocolysis for uterine contractions. Three women had mild pulmonary edema and required supplemental oxygen for less than 48 hours. Uterine puncture resulted in ultrasonographically detectable chorioamnionic separation in 7 of 11 women (64 percent), and all 11 women who underwent fetal tracheal occlusion had preterm premature rupture of the membranes, as compared with 3 of 13 women (23 percent) who received standard care (P<0.001) (Table 2Table 2
Pregnancy Outcomes and Complications According to the Actual Treatment.). In the tracheal-occlusion group, preterm premature rupture of the membranes did not lead to immediate delivery; the mean time from preterm premature rupture of the membranes to delivery was 9.5±8.5 days.All infants in the tracheal-occlusion group were delivered prematurely (by the planned ex utero intrapartum therapy procedure), as compared with 4 of 13 (31 percent) in the standard-care group (P<0.001). In the latter four cases, spontaneous premature labor developed, and the infants were delivered before the women could return to the University of California, San Francisco. Thus, the gestational age at delivery and the birth weight were significantly lower in the tracheal-occlusion group than in the standard-care group (P<0.001 for both comparisons) (Table 2). All women in both groups who desired subsequent pregnancies were able to conceive and carry to term healthy children (five women in the tracheal-occlusion group and four in the standard-care group).
Neonatal Outcomes
There was no significant difference in survival among infants between the standard-care group and the tracheal-occlusion group, whether the data were analyzed according to the actual treatment (10 of 13 infants, or 77 percent, survived, vs. 8 of 11, or 73 percent; P=1.00) or the assigned treatment (8 of 11, or 73 percent, vs. 10 of 13, or 77 percent; P=1.00) (Table 3Table 3
Ninety-Day Survival According to Assigned and Actual Treatment and According to the Lung-to-Head Ratio. and Figure 1Figure 1Kaplan–Meier Survival Curves for the Study Group as of November 1, 2002 (3.5 Years after Study Initiation).). The overall rate of survival at 90 days was 75 percent.Of the three infants in the standard-care group who died, two died before repair of their congenital diaphragmatic hernia (one from respiratory insufficiency at 4 days of age, and the other after withdrawal from life support at 1 day of age because of previously undiagnosed Fryn's syndrome), and the third died at 30 days of age from pulmonary hypertension. In the tracheal-occlusion group, all infants survived to repair of their congenital diaphragmatic hernia. Two infants died shortly after repair (one from respiratory insufficiency at 9 days, and the other from sepsis at 14 days); the third died at 71 days from pulmonary hypertension. One baby in each group died at more than 90 days of age, both from chronic pulmonary hypertension.
There was a nonsignificant inverse relation between gestational age at delivery and mortality. The gestational age at delivery was 34.9±3.4 weeks among survivors and 32.0±3.4 weeks among nonsurvivors (P=0.09). Analysis of pooled data from the two treatment groups revealed a direct association between the stratum of lung-to-head ratio and 90-day survival (Table 3).
To establish a more precise cutoff value for the lung-to-head ratio in order to predict survival, we stratified all the infants into two groups according to whether the lung-to-head ratio was low or high. We used receiver-operating-characteristic curves with cutoff values for the lung-to-head ratio of 0.85, 0.90, 0.95, and 1.0; a cutoff value of 0.90 resulted in the greatest area under the curve (0.78).
We used survival analysis with a censoring date of November 1, 2002 (3.5 years after initiation of the study), to identify the factors potentially affecting survival in this cohort. The treatment group was not a significant predictor of survival; the hazard ratio for death associated with tracheal occlusion, as compared with standard care, was 1.20 (95 percent confidence interval, 0.29 to 4.67). However, the lung-to-head ratio was a strong predictor of survival. The hazard ratio for death associated with a lung-to-head ratio greater than 0.90, as compared with a ratio less than or equal to 0.90, was 0.13 (95 percent confidence interval, 0.03 to 0.64).
Respiratory, Gastrointestinal, and Neurologic Outcomes
The rates of respiratory and gastrointestinal complications among survivors at discharge (at a mean of 60.9±23.5 days) are shown in Table 4Table 4
Respiratory and Gastrointestinal Outcomes According to the Treatment Group.. There were no significant differences between survivors in the tracheal-occlusion group and those in the standard-care group, despite the differences in gestational age at delivery. All infants required intensive respiratory support; one infant in the standard-care group received five days of extracorporeal membrane oxygenation before the repair was performed. There was no significant difference in age at the time of repair of congenital diaphragmatic hernia, the need for a prosthetic patch at repair of congenital diaphragmatic hernia, age at extubation, age at discharge, or the proportions of infants in the two treatment groups requiring supplemental oxygen. There was substantial gastrointestinal morbidity in both groups, with little difference between the groups.Seven infants (five receiving standard care and two undergoing tracheal occlusion) underwent computed tomographic imaging of the brain before discharge from the hospital; no abnormalities were seen. Ten infants underwent magnetic resonance imaging of the brain before discharge (four in the standard-care group and six in the tracheal-occlusion group); five infants had evidence of mild-to-moderate white-matter injury (three in the standard-care group and two in the tracheal-occlusion group). There were no detectable neurologic deficits on examination among survivors in either group at discharge.
Discussion
In this randomized, controlled study, a strategy to enhance lung growth before birth by occluding the fetal trachea proved no better than planned delivery and high-level neonatal care at a tertiary care center in improving the outcome for fetuses with severe congenital diaphragmatic hernia. The rate of survival among infants randomly assigned to treatment with fetal endoscopic tracheal occlusion (73 percent) met our expectations (predicted value, 77 percent) and was higher than the rate among historic controls (37 percent), but it proved no better than that among concurrent randomized controls.
The unexpectedly high survival rate in the group that received standard care (planned delivery and intensive postnatal care at a tertiary care center) led the data safety and monitoring board to conclude that even with further enrollment, the 90-day survival rates in the two groups would prove to be indistinguishable.
The higher-than-expected survival in the standard-care group may be due to the “trial effect.” The study design required that infants in both treatment groups be delivered, resuscitated, and intensively treated in a unit experienced in caring for critically ill newborns with pulmonary hyperplasia. Because “standard care” in this study was really optimal care (available at tertiary centers), conclusions about the general applicability of the trial results must be guarded.
Attempts to improve the outcome of severe congenital diaphragmatic hernia with treatments provided either before or after birth have proved to be double-edged swords. Intensive care after birth has improved survival but has increased long-term sequelae in survivors, and it is expensive.8,14-18 Intervention before birth may increase lung size, but prematurity caused by the intervention itself can be detrimental. In our small study, babies with severe congenital diaphragmatic hernia who underwent tracheal occlusion before birth were born at an average of 31 weeks of gestational age, as a consequence of the intervention. The finding that their rates of survival and respiratory outcomes (including the duration of oxygen supplementation) were similar to those among infants who did not undergo tracheal occlusion, who were born at an average of 37 weeks, suggests that any potential pulmonary benefits of tracheal occlusion were counterbalanced by adverse effects of earlier delivery on pulmonary function.
The results of our study underscore the importance of randomized trials in evaluating promising new therapies. This is the second NIH-sponsored trial of a new prenatal intervention for severe fetal congenital diaphragmatic hernia. The first trial showed that complete surgical repair of the anatomical defect (which required hysterotomy), although feasible, was no better than postnatal repair in improving survival and was ineffective when the liver as well as the bowel was herniated.26 That trial led to the abandonment of open complete repair at our institution and subsequently at centers around the world. Information derived from that trial led to the development of measures of the severity of pulmonary hypoplasia, including liver herniation and lung-to-head ratio. The failure of complete repair in that trial led to the development of an alternative physiological strategy to enlarge the hypoplastic fetal lung through temporary tracheal occlusion31 and to the development of less invasive fetal endoscopic techniques that did not require hysterotomy to achieve temporary, reversible tracheal occlusion.
Our ability to accurately diagnose and assess the severity of congenital diaphragmatic hernia before birth has improved dramatically. Fetuses with congenital diaphragmatic hernia and associated anomalies do poorly, whereas fetuses with isolated congenital diaphragmatic hernia, no liver herniation, and a lung-to-head ratio above 1.4 have an excellent prognosis (100 percent survival in our experience). In this study, which involved delivery at a tertiary care center, fetuses with a lung-to-head ratio between 0.9 and 1.4 had more than an 80 percent chance of survival. The small number of fetuses in both treatment groups with lung-to-head ratios of 0.9 or less had a poor prognosis.
It is possible that approaches to tracheal occlusion other than that used here might be beneficial. Although the duration of occlusion in this study (36.2±14.7 days) was similar to that used in animal models,35-39 the optimal timing and duration of occlusion in humans are not known. Short-term occlusion later in gestation and earlier occlusion (with possible reversal in utero) have been studied in animal models25-27 and applied in humans by ourselves and others. On the basis of the results of this trial, the Eurofoetus group is developing a randomized trial of fetoscopic endoluminal tracheal occlusion for fetuses with liver herniation and a lung-to-head ratio of less than 0.9 (Deprest J: personal communication). It is also possible that the risk of premature rupture of the membranes, leading to preterm labor and delivery, might be reduced by using smaller (2-mm) fetoscopes percutaneously and new techniques to seal the membranes, although these approaches require study.
The current findings demonstrate that fetal tracheal occlusion at 23 to 27 weeks of gestation to treat congenital diaphragmatic hernia is feasible with the use of minimally invasive fetoscopic techniques, but the results, in terms of fetal mortality and morbidity rates, are no better than those with postnatal care at a tertiary center. Fetuses with lung-to-head ratios of less than 0.9 have a low rate of survival and remain the focus for the development of new treatment strategies, either before or after birth.
Supported by a grant (R01 HL62433) from the National Institute of Child Health and Human Development, National Institutes of Health (to Dr. Albanese), by the Nicholson Fund, and by Glaser Pediatric Research Network.
We are indebted to the nurses, physicians, and support staff of the University of California, San Francisco, who provided superb care to the families in our study; to Dr. Christopher Dowd of Neuroradiology for balloon technology; to Dr. David Glidden for statistical support; to Stephanie Berman, M.S.W., for psychosocial evaluation; to Robin Bisgaard, R.N., for trial coordination and management; and to the staff of Ronald McDonald House of San Francisco.
Source Information
From the Fetal Treatment Center (M.R.H., S.B.H., J.A.K., P.L.S., D.L.F., H.L., R.A.F., J.A.F., C.T.A.), the Departments of Surgery (M.R.H., D.L.F., H.L., J.A.F., C.T.A.), Pediatrics (M.R.H., R.L.K., S.B.H., J.A.K., D.L.F., H.L., C.T.A.), Obstetrics, Gynecology and Reproductive Sciences (M.R.H., P.L.S., D.L.F., H.L., R.A.F., C.T.A.), and Radiology (R.A.F.), and the Cardiovascular Research Institute (R.L.K., J.A.K.), University of California, San Francisco, San Francisco.
Address reprint requests to Dr. Harrison at the University of California, San Francisco, Fetal Treatment Center, 513 Parnassus Ave., HSW-1601, San Francisco, CA 94143-0570, or at fetus@surgery.ucsf.edu.
Appendix
Data Safety Monitoring Board members included B.L. Short, M.D., R. O'Brien, Ph.D., H. Nielsen, M.D., L. Singer, M.D., and J. Frader, M.D.
- References
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Citing Articles
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Stephen C. O'Connor, Veronica J. Rooks, Alice Boyd Smith. (2012) Magnetic Resonance Imaging of the Fetal Central Nervous System, Head, Neck, and Chest. Seminars in Ultrasound, CT, and MRI 33:1, 86-101
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Jan Deprest, Paolo De Coppi. (2012) Antenatal management of isolated congenital diaphragmatic hernia today and tomorrow: ongoing collaborative research and development. Journal of Pediatric Surgery 47:2, 282-290
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Roberta L. Keller, Salvador Guevara-Gallardo, Diana L. Farmer. 2012. Surgical Disorders of the Chest and Airways. , 672-697.
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Nada Sudhakaran, Uma Sothinathan, Shailesh Patel. (2012) Best practice guidelines: Fetal surgery. Early Human Development 88:1, 15-19
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J. C. Jani, K. H. Nicolaides. (2012) Fetal surgery for severe congenital diaphragmatic hernia?. Ultrasound in Obstetrics & Gynecology 39:1, 7-9
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Tadaharu Okazaki, Nana Nakazawa, Yuki Ogasawara, Hiromichi Shoji, Toshiaki Shimizu, Shintaro Makino, Satoru Takeda, Geoffrey J. Lane, Atsuyuki Yamataka. (2011) Increase in fetal pulmonary artery diameters during late gestation is a predictor of outcome in congenital diaphragmatic hernia with liver herniation. Journal of Pediatric Surgery 46:12, 2254-2259
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Michele L. Lombardo, Debra J. Watson-Smith, Christopher S. Muratore, Stephen R. Carr, Barbara M. O'Brien, François I. Luks. (2011) Laser Ablation of Placental Vessels in Twin-to-Twin Transfusion Syndrome: A Paradigm for Endoscopic Fetal Surgery. Journal of Laparoendoscopic & Advanced Surgical Techniques 21:9, 869-872
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Ramin Kholdebarin, Barbara Maria Iwasiow, Richard Keijzer. (2011) Pulmonary development considerations in the surgical management of congenital diaphragmatic hernia. Early Human Development 87:11, 755-758
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N. Ochsenbein-Kölble. (2011) Invasive intrauterine Therapie. Der Gynäkologe
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Michał Szpinda, Marcin Daroszewski, Alina Woźniak, Anna Szpinda, Celestyna Mila-Kierzenkowska. (2011) Tracheal dimensions in human fetuses: an anatomical, digital and statistical study. Surgical and Radiologic Anatomy
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Citra N Mattar, Mahesh Choolani, Arijit Biswas, Simon N Waddington, Jerry KY Chan. (2011) Fetal gene therapy: recent advances and current challenges. Expert Opinion on Biological Therapy 11:10, 1257-1271
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, M. E. Brindle, M. Brar, E. D. Skarsgard. (2011) Patch repair is an independent predictor of morbidity and mortality in congenital diaphragmatic hernia. Pediatric Surgery International 27:9, 969-974
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Philip DeKoninck, Eduardo Gratacos, Tim Van Mieghem, Jute Richter, Paul Lewi, Ana Martin Ancel, Karel Allegaert, Kypros Nicolaides, Jan Deprest. (2011) Results of Fetal Endoscopic Tracheal Occlusion for congenital diaphragmatic hernia and the set up of the randomized controlled TOTAL trial. Early Human Development 87:9, 619-624
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J. R. Benjamin, M. J. Bizzarro, C. M. Cotten. (2011) Congenital Diaphragmatic Hernia: Updates and Outcomes. NeoReviews 12:8, e439-e452
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Beth M. Kline-Fath. (2011) Congenital diaphramatic hernia. Pediatric Radiology
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J. Jani, C. Valencia, M. Cannie, A. Vuckovic, M. Sellars, K.H. Nicolaides. (2011) Tracheal diameter at birth in severe congenital diaphragmatic hernia treated by fetal endoscopic tracheal occlusion. Prenatal Diagnosis 31:7, 699-704
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Malikah A. Alfaraj, Prakesh S. Shah, Desmond Bohn, Sophia Pantazi, Karel O'Brien, Priscilla P. Chiu, Rose Gaiteiro, Greg Ryan. (2011) Congenital diaphragmatic hernia: lung-to-head ratio and lung volume for prediction of outcome. American Journal of Obstetrics and Gynecology 205:1, 43.e1-43.e8
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Rubén A. Quintero, Luis F. Quintero, Ramen Chmait, Libardo Gómez Castro, Lisa M. Korst, Moshe Fridman, Eftichia V. Kontopoulos. (2011) The quantitative lung index (QLI): a gestational age−independent sonographic predictor of fetal lung growth. American Journal of Obstetrics and Gynecology
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A. Benachi, J. Saada, J. Martinovic, P. de Lagausie, L. Storme, J. Jani. (2011) Hernie congénitale du diaphragme : prise en charge anténatale. Revue des Maladies Respiratoires 28:6, 800-808
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Eric B. Jelin, Mozziyar Etemadi, Jose Encinas, Samuel C. Schecter, Cheryl Chapin, Jianfeng Wu, Salvador Guevara-Gallardo, Amar Nijagal, Kelly D. Gonzales, William T. Ferrier, Shuvo Roy, Doug Miniati. (2011) Dynamic tracheal occlusion improves lung morphometrics and function in the fetal lamb model of congenital diaphragmatic hernia. Journal of Pediatric Surgery 46:6, 1150-1157
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I. Sluiter, C.P. van de Ven, R.M.H. Wijnen, D. Tibboel. (2011) Congenital diaphragmatic hernia: Still a moving target. Seminars in Fetal and Neonatal Medicine 16:3, 139-144
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Darrell L. Cass. (2011) Impact of prenatal diagnosis and therapy on neonatal surgery. Seminars in Fetal and Neonatal Medicine 16:3, 130-138
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S. Speggiorin, A. Fierens, K. McHugh, D.J. Roebuck, C.A. McLaren, Q. Mok, M. Broadhead, M.J. Elliott. (2011) Bronchomegaly as a complication of fetal endoscopic tracheal occlusion. A caution and a possible solution. Journal of Pediatric Surgery 46:5, e1-e3
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Katherine E. Hartmann, Melissa L. McPheeters, Nancy C. Chescheir, Maria Gillam-Krakauer, J. Nikki McKoy, Rebecca Jerome, Nila A. Sathe, Laura Meints, William F. Walsh. (2011) Evidence to Inform Decisions About Maternal–Fetal Surgery. Obstetrics & Gynecology 117:5, 1191-1204
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Simpson, Joe Leigh, Greene, Michael F., . (2011) Fetal Surgery for Myelomeningocele?. New England Journal of Medicine 364:11, 1076-1077
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François I. Luks. (2011) New and/or improved aspects of fetal surgery. Prenatal Diagnosis 31:3, 252-258
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Y. Kitano, H. Okuyama, M. Saito, N. Usui, N. Morikawa, K. Masumoto, H. Takayasu, T. Nakamura, H. Ishikawa, M. Kawataki, S. Hayashi, N. Inamura, K. Nose, H. Sago. (2011) Re-evaluation of stomach position as a simple prognostic factor in fetal left congenital diaphragmatic hernia: a multicenter survey in Japan. Ultrasound in Obstetrics & Gynecology 37:3, 277-282
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Claire Brett, Peter J. Davis. 2011. Anesthesia for General Surgery in the Neonate. , 554-588.
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Kha Tran, David E. Cohen. 2011. Anesthesia for Fetal Surgery. , 589-604.
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Kha M. Tran. (2011) Anesthesia for Intrauterine Fetal Therapy and Ex Utero Intrapartum Therapy. Advances in Anesthesia 29:1, 129-148
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Noriaki Usui, Yoshihiro Kitano, Hiroomi Okuyama, Mari Saito, Nobuyuki Morikawa, Hajime Takayasu, Tomoo Nakamura, Satoshi Hayashi, Motoyoshi Kawataki, Hiroshi Ishikawa, Keisuke Nose, Noboru Inamura, Kouji Masumoto, Haruhiko Sago. (2011) Reliability of the lung to thorax transverse area ratio as a predictive parameter in fetuses with congenital diaphragmatic hernia. Pediatric Surgery International 27:1, 39-45
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Josilene Lobato, Carolina Nastri, Francisco Mauad Filho, Wellington Martins. (2011) [Diagnóstico pré-natal da hérnia diafragmática congênita] Prenatal diagnosis of congenital diafragmatic hernia. Experts in Ultrasound: Reviews and Perspectives 3:1, 11-15
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R. Ruano, C. T. Yoshisaki, M. M. da Silva, M. E. J. Ceccon, M. S. Grasi, U. Tannuri, M. Zugaib. (2011) A randomized controlled trial of fetal endoscopic tracheal occlusion versus postnatal management of severe isolated congenital diaphragmatic hernia. Ultrasound in Obstetrics & Gynecology20-27
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Daniel J. Ostlie, Shawn D. St Peter. (2010) The current state of evidence-based pediatric surgery. Journal of Pediatric Surgery 45:10, 1940-1946
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R. Douglas Wilson, Kerrie Lemerand, Mark P. Johnson, Alan W. Flake, Michael Bebbington, Holly L. Hedrick, N. Scott Adzick. (2010) Reproductive outcomes in subsequent pregnancies after a pregnancy complicated by open maternal-fetal surgery (1996–2007). American Journal of Obstetrics and Gynecology 203:3, 209.e1-209.e6
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Richard Keijzer, Prem Puri. (2010) Congenital diaphragmatic hernia. Seminars in Pediatric Surgery 19:3, 180-185
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Jan A. Deprest, Alan W. Flake, Eduard Gratacos, Yves Ville, Kurt Hecher, Kypros Nicolaides, Mark P. Johnson, François I. Luks, N. Scott Adzick, Michael R. Harrison. (2010) The making of fetal surgery. Prenatal Diagnosis 30:7, 653-667
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Nick Lansdale, Sabrina Alam, Paul D. Losty, Edwin C. Jesudason. (2010) Neonatal Endosurgical Congenital Diaphragmatic Hernia Repair. Annals of Surgery 252:1, 20-26
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V. Jain, S. Agarwala, V. Bhatnagar. (2010) Recent advances in the management of congenital diaphragmatic hernia. The Indian Journal of Pediatrics 77:6, 673-678
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Jeremy R. Grushka, Saleh Al-Abbad, Robert Baird, Pramod Puligandla, Feige Kaplan, Jean-Martin Laberge. (2010) The effect of in vitro tracheal occlusion on branching morphogenesis in fetal lung explants from the rat nitrofen model of congenital diaphragmatic hernia. Journal of Pediatric Surgery 45:5, 943-947
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D. Mullassery, M. E. Ba'ath, E. C. Jesudason, P. D. Losty. (2010) Value of liver herniation in prediction of outcome in fetal congenital diaphragmatic hernia: a systematic review and meta-analysis. Ultrasound in Obstetrics and Gynecology 35:5, 609-614
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V. Beck, A. Pexsters, L. Gucciardo, T. Mieghem, I. Sandaite, S. Rusconi, Ph DeKoninck, K. Srisupundit, K. O. Kagan, Jan Deprest. (2010) The use of endoscopy in fetal medicine. Gynecological Surgery 7:2, 113-125
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Julien Saada, Noufissa Oudrhiri, Arnaud Bonnard, Pascal de Lagausie, Abderrahim Aissaoui, Michelle Hauchecorne, Jean-François Oury, Yves Aigrain, Michel Peuchmaur, Jean-Marie Lehn, Pierre Lehn, Dominique Luton. (2010) Combining keratinocyte growth factor transfection into the airways and tracheal occlusion in a fetal sheep model of congenital diaphragmatic hernia. The Journal of Gene Medicine 12:5, 413-422
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Jan Deprest, Luc Breysem, Eduardo Gratacos, Kypros Nicolaides, Filip Claus, Anne Debeer, Maria Helena Smet, Marijke Proesmans, Pierre Fayoux, Laurent Storme. (2010) Tracheal side effects following fetal endoscopic tracheal occlusion for severe congenital diaphragmatic hernia. Pediatric Radiology 40:5, 670-673
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M. Yamamoto, Y. Ville. (2010) Fetal lung assessment in congenital diaphragmatic hernia: evidence for growth. Ultrasound in Obstetrics and Gynecology 35:5, 522-524
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Kieran McHugh, Asim Afaq, Nigel Broderick, Hany O. Gabra, Derek J. Roebuck, Martin J. Elliott. (2010) Tracheomegaly: a complication of fetal endoscopic tracheal occlusion in the treatment of congenital diaphragmatic hernia. Pediatric Radiology 40:5, 674-680
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Angela C Rossi. (2010) Indications and outcomes of intrauterine surgery for fetal malformations. Current Opinion in Obstetrics and Gynecology 22:2, 159-165
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Murat Kemal Cigdem, Goksel Kizil, Abdurrahman Onen, Murat Kizil, Yusuf Nergiz, Yusuf Celik. (2010) Is there a role for antioxidants in prevention of pulmonary hypoplasia in nitrofen-induced rat model of congenital diaphragmatic hernia?. Pediatric Surgery International 26:4, 401-406
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Susan T. Mahan, James R. Kasser. (2010) Prenatal Ultrasound for Diagnosis of Orthopaedic Conditions. Journal of Pediatric Orthopaedics 30, S35-S39
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R. Papanna, S. Molina, K. Y. Moise, K. J. Moise Jr, A. Johnson. (2010) Chorioamnion plugging and the risk of preterm premature rupture of membranes after laser surgery in twin-twin transfusion syndrome. Ultrasound in Obstetrics and Gynecology 35:3, 337-343
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MARC VAN DE VELDE, FREDERIK DE BUCK, TIM VAN MIEGHEM, LEONARDO GUCCIARDO, PHILIP DE KONINCK, JAN DEPREST. (2010) FETAL ANAESTHESIA: IS THIS NECESSARY FOR FETOSCOPIC THERAPY?. Fetal and Maternal Medicine Review 21:01, 24
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Jan A. Deprest, Roland Devlieger, Kasemsri Srisupundit, Veronika Beck, Inga Sandaite, Silvia Rusconi, Filip Claus, Gunnar Naulaers, Marc Van de Velde, Paul Brady, Koen Devriendt, Joris Vermeesch, Jaan Toelen, Marianne Carlon, Zeger Debyser, Luc De Catte, Liesbeth Lewi. (2010) Fetal surgery is a clinical reality. Seminars in Fetal and Neonatal Medicine 15:1, 58-67
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Holly L. Hedrick. (2010) Management of prenatally diagnosed congenital diaphragmatic hernia. Seminars in Fetal and Neonatal Medicine 15:1, 21-27
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Grozdana Bilic, Carrie Brubaker, Phillip B. Messersmith, Ajit S. Mallik, Thomas M. Quinn, Claudia Haller, Elisa Done, Leonardo Gucciardo, Steffen M. Zeisberger, Roland Zimmermann, Jan Deprest, Andreas H. Zisch. (2010) Injectable candidate sealants for fetal membrane repair: bonding and toxicity in vitro. American Journal of Obstetrics and Gynecology 202:1, 85.e1-85.e9
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Alexandra Benachi. 2010. Pathologies pulmonaires et diaphragme. , 87-100.
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Rodrigo Ruano, Marie-Cécile Aubry, Bruno Barthe, Yves Dumez, Alexandra Benachi. (2009) Three-dimensional ultrasonographic measurements of the fetal lungs for prediction of perinatal outcome in isolated congenital diaphragmatic hernia. Journal of Obstetrics and Gynaecology Research 35:6, 1031-1041
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S Grisaru-Granovsky, R Rabinowitz, A Ioscovich, D Elstein, MS Schimmel. (2009) Congenital diaphragmatic hernia: review of the literature in reflection of unresolved dilemmas. Acta Paediatrica 98:12, 1874-1881
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Anne Greenough. (2009) Prenatal factors in the development of chronic lung disease. Seminars in Fetal and Neonatal Medicine 14:6, 339-344
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Nigel J. Hall, Simon Eaton, Agostino Pierro. (2009) The evidence base for neonatal surgery. Early Human Development 85:11, 713-718
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Chang Xu, Wenying Liu, Zhongxian Chen, Yuanxiang Wang, Zhongxun Xiong, Yi Ji. (2009) Effect of prenatal tetrandrine administration on transforming growth factor-β1 level in the lung of nitrofen-induced congenital diaphragmatic hernia rat model. Journal of Pediatric Surgery 44:8, 1611-1620
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Gong Chen, Shan Zheng, Xian Min Xiao, Yi Luo. (2009) The impact of iatrogenic gastroschisis on pulmonary maturation in the fetal rabbit models of congenital diaphragmatic hernia. Pediatric Surgery International 25:7, 635-640
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Tim Jancelewicz, Michael R. Harrison. (2009) A History of Fetal Surgery. Clinics in Perinatology 36:2, 227-236
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Jan A. Deprest, Eduardo Gratacos, Kypros Nicolaides, Elise Done, Tim Van Mieghem, Leonardo Gucciardo, Filip Claus, Anne Debeer, Karel Allegaert, Irwin Reiss, Dick Tibboel. (2009) Changing Perspectives on the Perinatal Management of Isolated Congenital Diaphragmatic Hernia in Europe. Clinics in Perinatology 36:2, 329-347
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Emily F. Durkin, Aimen Shaaban. (2009) Commonly Encountered Surgical Problems in the Fetus and Neonate. Pediatric Clinics of North America 56:3, 647-669
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V. Kandice Mah, Mohammed Zamakhshary, Doug Y. Mah, Brian Cameron, Juan Bass, Desmond Bohn, Leslie Scott, Sharifa Himidan, Mark Walker, Peter C.W. Kim. (2009) Absolute vs relative improvements in congenital diaphragmatic hernia survival: what happened to “hidden mortality”. Journal of Pediatric Surgery 44:5, 877-882
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Anthony S. Buys Roessingh, Anh Tuan Dinh-Xuan. (2009) Congenital diaphragmatic hernia: current status and review of the literature. European Journal of Pediatrics 168:4, 393-406
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Jose L. Peiró, Elena Carreras, Gabriela Guillén, Silvia Arévalo, M. Angeles Sánchez-Durán, Teresa Higueras, Felix Castillo, Claudia Marhuenda, Josep Lloret, Vicenç Martínez-Ibáñez. (2009) Therapeutic Indications of Fetoscopy: A 5-Year Institutional Experience. Journal of Laparoendoscopic & Advanced Surgical Techniques 19:2, 229-236
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Kevin C. Worley, Jodi S. Dashe, Robert G. Barber, Stephen M. Megison, Donald D. McIntire, Diane M. Twickler. (2009) Fetal magnetic resonance imaging in isolated diaphragmatic hernia: volume of herniated liver and neonatal outcome. American Journal of Obstetrics and Gynecology 200:3, 318.e1-318.e6
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Justin D Klein, Carol E Barnewolt, Russell W Jennings. (2009) Current and future treatment of fetal thoracic masses. Expert Review of Obstetrics & Gynecology 4:2, 201-217
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Chandrasen K. Sinha, Saidul Islam, Shailesh Patel, Kypros Nicolaides, Anne Greenough, Mark Davenport. (2009) Congenital diaphragmatic hernia: prognostic indices in the fetal endoluminal tracheal occlusion era. Journal of Pediatric Surgery 44:2, 312-316
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Jan A. Deprest, Andreas W. Flemmer, Eduard Gratacos, Kypros Nicolaides. (2009) Antenatal prediction of lung volume and in-utero treatment by fetal endoscopic tracheal occlusion in severe isolated congenital diaphragmatic hernia. Seminars in Fetal and Neonatal Medicine 14:1, 8-13
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Frederick J. Rescorla. (2009) What's New in Pediatric Surgery. Journal of Pediatric Surgery 44:1, 43-52
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J. A. Deprest, J. A. Hyett, A. W. Flake, K. Nicolaides, E. Gratacos. (2009) Current controversies in prenatal diagnosis 4: Should fetal surgery be done in all cases of severe diaphragmatic hernia?. Prenatal Diagnosis 29:1, 15-19
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M. G. Peetsold, H. A. Heij, C. M. F. Kneepkens, A. F. Nagelkerke, J. Huisman, R. J. B. J. Gemke. (2009) The long-term follow-up of patients with a congenital diaphragmatic hernia: a broad spectrum of morbidity. Pediatric Surgery International 25:1, 1-17
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Lisa R. Bomgaars, Stacey L. Berg, Ann R. Stark. 2009. Pediatrics. , 497-507.
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Cassandra Willyard. (2008) Tinkering in the womb: the future of fetal surgery. Nature Medicine 14:11, 1176-1177
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Karl-Ludwig Waag, Steffan Loff, Katrin Zahn, Mansour Ali, Steffen Hien, Markus Kratz, Wolfgang Neff, Regine Schaffelder, Thomas Schaible. (2008) Congenital diaphragmatic hernia: a modern day approach. Seminars in Pediatric Surgery 17:4, 244-254
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Aimee C. Pastor, J. Duncan Phillips, Stephen J. Fenton, Rebecka L. Meyers, Amy W. Lamm, Mehul V. Raval, Elizabeth Lehman, Tracy B. Karp, Paul W. Wales, Jacob C. Langer. (2008) Routine use of a SILASTIC spring-loaded silo for infants with gastroschisis: a multicenter randomized controlled trial. Journal of Pediatric Surgery 43:10, 1807-1812
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Enrico Danzer, Marcus G. Davey, Portia A. Kreiger, Eduardo D. Ruchelli, Mark P. Johnson, N. Scott Adzick, Alan W. Flake, Holly L. Hedrick. (2008) Fetal tracheal occlusion for severe congenital diaphragmatic hernia in humans: a morphometric study of lung parenchyma and muscularization of pulmonary arterioles. Journal of Pediatric Surgery 43:10, 1767-1775
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Robert Baird, Nasir Khan, Helene Flageole, Mark Anselmo, Pramod Puligandla, Jean-Martin Laberge. (2008) The Effect of Tracheal Occlusion on Lung Branching in the Rat Nitrofen CDH Model. Journal of Surgical Research 148:2, 224-229
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Sandra Montedonico, Nana Nakazawa, Prem Puri. (2008) Congenital diaphragmatic hernia and retinoids: searching for an etiology. Pediatric Surgery International 24:7, 755-761
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Priscilla Chiu, Holly L. Hedrick. (2008) Postnatal management and long-term outcome for survivors with congenital diaphragmatic hernia. Prenatal Diagnosis 28:7, 592-603
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Elisa Doné, Leonardo Gucciardo, Tim Van Mieghem, Jacques Jani, Mieke Cannie, Dominique Van Schoubroeck, Roland Devlieger, Luc De Catte, Philipp Klaritsch, Steffi Mayer, Veronika Beck, Anne Debeer, Eduardo Gratacos, Kypros Nicolaides, Jan Deprest. (2008) Prenatal diagnosis, prediction of outcome and in utero therapy of isolated congenital diaphragmatic hernia. Prenatal Diagnosis 28:7, 581-591
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Jan A Deprest, Elisa Done, Tim Van Mieghem, Leonardo Gucciardo. (2008) Fetal surgery for anesthesiologists. Current Opinion in Anaesthesiology 21:3, 298-307
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Marcus Davey, Shincy Shegu, Enrico Danzer, Eduardo Ruchelli, Scott Adzick, Alan Flake, Holly L. Hedrick. (2007) Pulmonary arteriole muscularization in lambs with diaphragmatic hernia after combined tracheal occlusion/glucocorticoid therapy. American Journal of Obstetrics and Gynecology 197:4, 381.e1-381.e7
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