Fetal MR Lung Volumetry in Congenital Diaphragmatic Hernia (CDH): Prediction of Clinical Outcome and the Need for Extracorporeal Membrane Oxygenation (ECMO)

Abstract

Background: Despite the ultrasound (US) based lung-to-head ratio (LHR) and first results of fetal lung volume (FLV) determination in magnetic resonance imaging (MRI), there is no reliable prenatal parameter for the clinical course and outcome of fetuses with congenital diaphragmatic hernia (CDH), in particular for the need of extracorporeal membrane oxygenation (ECMO).

Patients and Method: MR FLV measurement was evaluated in 36 fetuses with CDH using T2-weighted half-Fourier acquisition single-shot turbo spin echo (HASTE) imaging. FLV and liver herniation, respectively, were correlated with survival and the need for ECMO therapy. A total of 18 healthy fetuses served as controls. MR FLV measurement was applied to predict survival and the need for neonatal ECMO therapy and to assess liver herniation as a prognostic parameter.

Results: On MRI there was a highly significant correlation of the FLV and patients’ survival (p=0.0001) and ECMO requirement, respectively (p=0.0029). Compared to normal controls mean FLV in infants who died was 10% (9.4±5.8 ml) and 32% in surviving infants (25±9.7 ml). Liver herniation significantly decreased lung volume and negatively impacted clinical outcome (p<0.0005).

Conclusion: The MR FLV is a strong predictor of survival in CDH patients. MR FLV measurements are also valuable to identify patients who may benefit from ECMO therapy. Upward liver herniation is the most important additional prognostic parameter.

Zusammenfassung

Hintergrund: Trotz der Nutzung der sonografischen (US) ‘lung to head’ ratio (LHR) und ersten Ergebnissen der Bestimmung des fetalen Lungenvolumens (FLV) in der Magnetresonanztomografie (MR), existiert kein zuverlässiger pränataler Parameter für den klinischen Verlauf von Feten mit einer kongenitalen Zwerchfellhernie (CDH), insbesondere nicht für die Notwendigkeit einer extrakorporalen Membranoxygenierungs- (ECMO)-Therapie.

Patienten und Methoden: Die Quantifizierung des MR-FLV wurde bei 36 Feten mit einer CDH untersucht. Benutzt zur MR-Bildgebung wurde eine T2-gewichtete ,half-Fourier acquisition single-shot turbo spin echo'-(HASTE)-Sequenz. Das FLV und die Verlagerung der Leber wurden mit dem Überleben der Kinder und der Notwendigkeit einer ECMO-Therapie korreliert. 18 gesunde Feten dienten als altersentsprechende Kontrollgruppe. Die Messung des MR-FLV wurde zur Prognosebeurteilung für Überleben und Notwendigkeit einer ECMO-Therapie benutzt. Die Verlagerung der Leber wurde als prognostischer Parameter beurteilt.

Ergebnisse: Die Magnetresonanztomografie zeigte eine hochsignifikante Korrelation zwischen FLV und dem Überleben der Patienten (p=0,0001) und der Notwendigkeit einer ECMO-Therapie (p=0,0029). Verglichen mit normalen Kontrollen beträgt das mittlere FLV von verstorbenen Kindern 10% (9,4±5,8 ml) und für überlebende Kinder 32% (25±9,7 ml). Die Hernierung der Leber führt zu einer signifikanten Reduktion des FLVs und verschlechtert den klinischen Verlauf (p<0,0005).

Schlussfolgerung: Das MR-FLV ist ein höchst valider Parameter zur Vorhersage des Überlebens bei Patienten mit einer CDH. Die Messung des MR-FLV ist wertvoll, um Patienten zu identifizieren, die von einer ECMO-Therapie profitieren können. Die Hernierung der Leber nach intrathorakal ist der wichtigste zusätzliche prognostische Parameter.

congenital diaphragmatic hernia - extracorporeal membrane oxygenation - fetal lung volume measurement - magnetic resonance imaging

kongenitale Zwerchfellhernie - extrakorporale Membranoxygenierung - fetales Lungenvolumen - Magnetresonanztomografie

References

• 1 Albanese CT, Lopoo J, Goldstein RB. et al . Fetal liver position and perinatal outcome for congenital diaphragmatic hernia.  Prenat Diagn. 1998;  18 1138-1142
• 2 Arkovitz MS, Russo M, Devine P. et al . Fetal lung-head ratio is not related to outcome for antenatal diagnosed congenital diaphragmatic hernia.  J Pediatr Surg. 2007;  42 107-110 , discussion 110–111
• 3 Bagolan P, Casaccia G, Crescenzi F. et al . Impact of a current treatment protocol on outcome of high-risk congenital diaphragmatic hernia.  J Pediatr Surg. 2004;  39 313-318 , discussion 313–318
• 4 Barnewolt CE, Kunisaki SM, Fauza DO. et al . Percent predicted lung volumes as measured on fetal magnetic resonance imaging: a useful biometric parameter for risk stratification in congenital diaphragmatic hernia.  J Pediatr Surg. 2007;  42 193-197
• 5 Bedoyan JK, Blackwell SC, Treadwell MC. et al . Congenital diaphragmatic hernia: associated anomalies and antenatal diagnosis. Outcome-related variables at two Detroit hospitals.  Pediatr Surg Int. 2004;  20 170-176
• 6 Bohn D. Congenital diaphragmatic hernia.  Am J Respir Crit Care Med. 2004;  166 911-915
• 7 Boloker J, Bateman DA, Wung JT. et al . Congenital diaphragmatic hernia in 120 infants treated consecutively with permissive hypercapnea/spontaneous respiration/elective repair.  J Pediatr Surg. 2002;  37 357-366
• 8 Bonfils M, Emeriaud G, Durand C. et al . Fetal lung volume in congenital diaphragmatic hernia.  Arch Dis Child Fetal Neonatal Ed. 2006;  91 F363-4
• 9 Breysem L, Bosmans H, Dymarkowski S. et al . The value of fast MR imaging as an adjunct to ultrasound in prenatal diagnosis.  Eur Radiol. 2003;  13 1538-1548
• 10 Bronshitein M, Lewit N, Sujov PO. et al . Prenatal diagnosis of congenital diaphragmatic hernia: timing of visceral herniation and outcome.  Prenat Diagn. 1995;  15 695-698
• 11 Bulas D, Glass P. Neonatal ECMO: neuroimaging and neurodevelopmental outcome.  Semin Perinatol. 2005;  29 58-65
• 12 Coakley FV, Lopoo JB, Lu Y. et al . Normal and hypoplastic fetal lungs: volumetric assessment with prenatal single-shot rapid acquisition with relaxation enhancement MR imaging.  Radiology. 2000;  216 107-111
• 13 D’Agostino JA, Bernbaum JC, Gerdes M. et al . Outcome for infants with congenital diaphragmatic hernia requiring extracorporeal membrane oxygenation: the first year.  J Pediatr Surg. 1995;  30 10-15
• 14 Devine PC, Malone FD. Noncardiac thoracic anomalies.  Clin Perinatol. 2000;  27 865-899
• 15 Downard CD, Jaksic T, Garza JJ. et al . Analysis of an improved survival rate for congenital diaphragmatic hernia.  J Pediatr Surg. 2003;  38 729-732
• 16 Farrell T, Leslie JR, Chien PF. et al . The reliability and validity of three dimensional ultrasound volumetric measurements using an in vitro balloon and in vivo uterine model.  Bjog. 2001;  108 573-582
• 17 Gorincour G, Bouvenot J, Mourot MG. et al . Prenatal prognosis of congenital diaphragmatic hernia using magnetic resonance imaging measurement of fetal lung volume.  Ultrasound Obstet Gynecol. 2005;  26 738-744
• 18 Harrison MR, Mychaliska GB, Albanese CT. et al . Correction of congenital diaphragmatic hernia in utero IX: fetuses with poor prognosis (liver herniation and low lung-to-head ratio) can be saved by fetoscopic temporary tracheal occlusion.  J Pediatr Surg. 1998;  33 1017-1022
• 19 Hayakawa M, Seo T, Itakura A. et al . The MRI findings of the right-sided fetal lung can be used to predict postnatal mortality and the requirement for extracorporeal membrane oxygenation in isolated left-sided congenital diaphragmatic hernia.  Pediatr Res. 2007;  62 93-97
• 20 Heling KS, Wauer RR, Hammer H. et al . Reliability of the lung-to-head ratio predicting outcome and neonatal ventilation parameters in fetuses with congenital diaphragmatic hernia.  Ultrasound Obstet Gynecol. 2005;  25 112-118
• 21 Hellmeyer L, Ballast A, Tekesin I. et al . Evaluation of the development of lung hypoplasia in the premature lamb.  Arch Gynecol Obstet. 2005;  271 231-234
• 22 Jani J, Breysem L, Maes F. et al . Accuracy of magnetic resonance imaging for measuring fetal sheep lungs and other organs.  Ultrasound Obstet Gynecol. 2005;  25 270-276
• 23 Jani J, Peralta CF, Schoubroeck D Van. et al . Relationship between lung-to-head ratio and lung volume in normal fetuses and fetuses with diaphragmatic hernia.  Ultrasound Obstet Gynecol. 2006;  27 545-550
• 24 Jani JC, Nicolaides KH, Gratacos E. et al . Fetal lung-to-head ratio in the prediction of survival in severe left-sided diaphragmatic hernia treated by fetal endoscopic tracheal occlusion (FETO).  Am J Obstet Gynecol. 2006;  195 1646-1650
• 25 Javid PJ, Jaksic T, Skarsgard ED. et al . Survival rate in congenital diaphragmatic hernia: the experience of the Canadian Neonatal Network.  J Pediatr Surg. 2004;  39 657-660
• 26 Kalache KD, Espinoza J, Chaiworapongsa T. et al . Three-dimensional ultrasound fetal lung volume measurement: a systematic study comparing the multiplanar method with the rotational (VOCAL) technique.  Ultrasound Obstet Gynecol. 2003;  21 111-118
• 27 Kohl T, Gembruch U, Filsinger B. et al . Encouraging early clinical experience with deliberately delayed temporary fetoscopic tracheal occlusion for the prenatal treatment of life-threatening right and left congenital diaphragmatic hernias.  Fetal Diagn Ther. 2006;  21 314-318
• 28 Langham  Jr  MR, Kays DW, Beierle EA. et al . Twenty years of progress in congenital diaphragmatic hernia at the University of Florida.  Am Surg. 2003;  69 45-52
• 29 Laudy JA, Gucht M Van, Dooren MF Van. et al . Congenital diaphragmatic hernia: an evaluation of the prognostic value of the lung-to-head ratio and other prenatal parameters.  Prenat Diagn. 2003;  23 634-639
• 30 Lewis DA, Reickert C, Bowerman R. et al . Prenatal ultrasonography frequently fails to diagnose congenital diaphragmatic hernia.  J Pediatr Surg. 1997;  32 352-356
• 31 Lipshutz GS, Albanese CT, Feldstein VA. et al . Prospective analysis of lung-to-head ratio predicts survival for patients with prenatally diagnosed cengenital diaphragmatic hernia.  J Pediatr Surg. 1997;  32 1634-1636
• 32 Mahieu-Caputo D, Sonigo P, Dommergues M. et al . Fetal lung volume measurement by magnetic resonance imaging in congenital diaphragmatic hernia.  Bjog. 2001;  108 863-868
• 33 MacGahren ED, Mallik K, Rodgers BM. Neurological outcome is diminished in survivors of congenital diaphragmatic hernia requiring extracorporeal membrane oxygenation.  J Pediatr Surg. 1997;  32 1216-1220
• 34 Metkus AP, Filly RA, Stringer MD. et al . Sonographic predictors of survival in fetal diaphragmatic hernia.  J Pediatr Surg. 1996;  31 148-151
• 35 Moeglin D, Talmant C, Duyme M. et al . Fetal lung volumetry using two- and three-dimensional ultrasound.  Ultrasound Obstet Gynecol. 2005;  25 119-127
• 36 Moya FR, Lally KP. Evidence-based management of infants with congenital diaphragmatic hernia.  Semin Perinatol. 2005;  29 112-117
• 37 Paek BW, Coakley FV, Lu Y. et al . Congenital diaphragmatic hernia: prenatal evaluation with MR lung volumetry – preliminary experience.  Radiology. 2001;  220 63-67
• 38 Peralta CF, Cavoretto P, Csapo B. et al . Lung and heart volumes by three-dimensional ultrasound in normal fetuses at 12–32 weeks’ gestation.  Ultrasound Obstet Gynecol. 2006;  27 128-133
• 39 Raine-Fenning NJ, Clewes JS, Kendall NR. et al . The interobserver reliability and validity of volume calculation from three-dimensional ultrasound datasets in the in vitro setting.  Ultrasound Obstet Gynecol. 2003;  21 283-291
• 40 Riccabona M, Nelson TR, Pretorius DH. et al . Three-dimensional ultrasound: accuracy of distance and volume measurements.  Ultrasound Obstet Gynecol. 1996;  7 429-434
• 41 Ruano R, Joubin L, Sonigo P. et al . Fetal lung volume estimated by 3-dimensional ultrasonography and magnetic resonance imaging in cases with isolated congenital diaphragmatic hernia.  J Ultrasound Med. 2004;  23 353-358
• 42 Ruano R, Benachi A, Joubin L. et al . Three-dimensional ultrasonographic assessment of fetal lung volume as prognostic factor in isolated congenital diaphragmatic hernia.  Bjog. 2004;  111 423-429
• 43 Ruano R, Martinovic J, Dommergues M. et al . Accuracy of fetal lung volume assessed by three-dimensional sonography.  Ultrasound Obstet Gynecol. 2005;  26 725-730
• 44 Ruano R, Joubin L, Aubry MC. et al . A nomogram of fetal lung volumes estimated by 3-dimensional ultrasonography using the rotational technique (virtual organ computer-aided analysis).  J Ultrasound Med. 2006;  25 701-709
• 45 Sabogal JC, Becker E, Bega G. et al . Reproducibility of fetal lung volume measurements with 3-dimensional ultrasonography.  J Ultrasound Med. 2004;  23 347-352
• 46 Sbragia L, Paek BW, Filly RA. et al . Congenital diaphragmatic hernia without herniation of the liver: does the lung-to-head ratio predict survival?.  J Ultrasound Med. 2000;  19 845-848
• 47 Shaw KS, Filiatrault D, Yazbeck S. et al . Improved survival for congenital diaphragmatic hernia, based on prenatal ultrasound diagnosis and referral to a combined obstetric-pediatric surgical center.  J Pediatr Surg. 1994;  29 1268-1269
• 48 Skari H, Bjornland K, Haugen G. et al . Congenital diaphragmatic hernia: a meta-analysis of mortality factors.  J Pediatr Surg. 2000;  35 1187-1197
• 49 Stevens TP, Chess PR, MacConnochie KM. et al . Survival in early- and late-term infants with congenital diaphragmatic hernia treated with extracorporeal membrane oxygenation.  Pediatrics. 2002;  110 590-596
• 50 Tibboel D, Gaag AV. Etiologic and genetic factors in congenital diaphragmatic hernia.  Clin Perinatol. 1996;  23 689-699
• 51 Walsh DS, Hubbard AM, Olutoye OO. et al . Assessment of fetal lung volumes and liver herniation with magnetic resonance imaging in congenital diaphragmatic hernia.  AM J Obstet Gynecol. 2000;  183 1067-1069
• 52 Ward VL, Nishino M, Hatabu H. et al . Fetal lung volume measurements: determination with MR imaging–effect of various factors.  Radiology. 2006;  240 187-193
• 53 Williams G, Coakley FV, Qayyum A. et al . Fetal relative lung volume: quantification by using prenatal MR imaging lung volumetry.  Radiology. 2004;  233 457-462
• 54 The collaborative UK ECMO . (Extracorporeal Membrane Oxygenation) trial: follow-up to 1 year of age.  Pediatrics. 1998;  101 E1
• 55 Does extracorporeal membrane oxygenation improve survival in neonates with congenital diaphragmatic hernia? The Congenital Diaphragmatic Hernia Study Group.  J Pediatr Surg. 1999;  34 720-724

1 equal contribution.

Correspondence