Standardization of Sonographic Lung-to-Head Ratio Measurements in Isolated Congenital Diaphragmatic Hernia
Impact on the Reproducibility and Efficacy to Predict Outcomes
Ingrid Schwach Werneck Britto MD,PhD
Texas Children's Fetal Center, Houston, Texas USA
Department of Obstetrics and Gynecology, Baylor College of Medicine, Houston, Texas USA
Search for more papers by this authorNicolas Sananes MD
Texas Children's Fetal Center, Houston, Texas USA
Department of Obstetrics and Gynecology, Baylor College of Medicine, Houston, Texas USA
Search for more papers by this authorOluyinka O. Olutoye MD,PhD
Texas Children's Fetal Center, Houston, Texas USA
Michael E. DeBakey Department of Surgery, Baylor College of Medicine, Houston, Texas USA
Search for more papers by this authorDarrell L. Cass MD
Texas Children's Fetal Center, Houston, Texas USA
Michael E. DeBakey Department of Surgery, Baylor College of Medicine, Houston, Texas USA
Search for more papers by this authorHaleh Sangi-Haghpeykar PhD
Department of Obstetrics and Gynecology, Baylor College of Medicine, Houston, Texas USA
Search for more papers by this authorTimothy C. Lee MD
Texas Children's Fetal Center, Houston, Texas USA
Michael E. DeBakey Department of Surgery, Baylor College of Medicine, Houston, Texas USA
Search for more papers by this authorChristopher I. Cassady MD
Texas Children's Fetal Center, Houston, Texas USA
Department of Radiology, Baylor College of Medicine, Houston, Texas USA
Search for more papers by this authorAmy Mehollin-Ray MD
Texas Children's Fetal Center, Houston, Texas USA
Department of Radiology, Baylor College of Medicine, Houston, Texas USA
Search for more papers by this authorStephen Welty MD
Department of Radiology, Baylor College of Medicine, Houston, Texas USA
Department of Pediatrics, Section of Neonatology, Baylor College of Medicine, Houston, Texas USA
Search for more papers by this authorCaraciolo Fernandes MD
Texas Children's Fetal Center, Houston, Texas USA
Department of Pediatrics, Section of Neonatology, Baylor College of Medicine, Houston, Texas USA
Search for more papers by this authorMichael A. Belfort MD,PhD
Texas Children's Fetal Center, Houston, Texas USA
Department of Obstetrics and Gynecology, Baylor College of Medicine, Houston, Texas USA
Search for more papers by this authorWesley Lee MD
Texas Children's Fetal Center, Houston, Texas USA
Department of Obstetrics and Gynecology, Baylor College of Medicine, Houston, Texas USA
Search for more papers by this authorCorresponding Author
Rodrigo Ruano MD,PhD
Texas Children's Fetal Center, Houston, Texas USA
Department of Obstetrics and Gynecology, Baylor College of Medicine, Houston, Texas USA
Address correspondence to Rodrigo Ruano, MD, PhD, Pavilion for Women, Texas Children's Fetal Center, 6651 Main St, Suite F1020, Houston, TX 77030 USA.Search for more papers by this authorIngrid Schwach Werneck Britto MD,PhD
Texas Children's Fetal Center, Houston, Texas USA
Department of Obstetrics and Gynecology, Baylor College of Medicine, Houston, Texas USA
Search for more papers by this authorNicolas Sananes MD
Texas Children's Fetal Center, Houston, Texas USA
Department of Obstetrics and Gynecology, Baylor College of Medicine, Houston, Texas USA
Search for more papers by this authorOluyinka O. Olutoye MD,PhD
Texas Children's Fetal Center, Houston, Texas USA
Michael E. DeBakey Department of Surgery, Baylor College of Medicine, Houston, Texas USA
Search for more papers by this authorDarrell L. Cass MD
Texas Children's Fetal Center, Houston, Texas USA
Michael E. DeBakey Department of Surgery, Baylor College of Medicine, Houston, Texas USA
Search for more papers by this authorHaleh Sangi-Haghpeykar PhD
Department of Obstetrics and Gynecology, Baylor College of Medicine, Houston, Texas USA
Search for more papers by this authorTimothy C. Lee MD
Texas Children's Fetal Center, Houston, Texas USA
Michael E. DeBakey Department of Surgery, Baylor College of Medicine, Houston, Texas USA
Search for more papers by this authorChristopher I. Cassady MD
Texas Children's Fetal Center, Houston, Texas USA
Department of Radiology, Baylor College of Medicine, Houston, Texas USA
Search for more papers by this authorAmy Mehollin-Ray MD
Texas Children's Fetal Center, Houston, Texas USA
Department of Radiology, Baylor College of Medicine, Houston, Texas USA
Search for more papers by this authorStephen Welty MD
Department of Radiology, Baylor College of Medicine, Houston, Texas USA
Department of Pediatrics, Section of Neonatology, Baylor College of Medicine, Houston, Texas USA
Search for more papers by this authorCaraciolo Fernandes MD
Texas Children's Fetal Center, Houston, Texas USA
Department of Pediatrics, Section of Neonatology, Baylor College of Medicine, Houston, Texas USA
Search for more papers by this authorMichael A. Belfort MD,PhD
Texas Children's Fetal Center, Houston, Texas USA
Department of Obstetrics and Gynecology, Baylor College of Medicine, Houston, Texas USA
Search for more papers by this authorWesley Lee MD
Texas Children's Fetal Center, Houston, Texas USA
Department of Obstetrics and Gynecology, Baylor College of Medicine, Houston, Texas USA
Search for more papers by this authorCorresponding Author
Rodrigo Ruano MD,PhD
Texas Children's Fetal Center, Houston, Texas USA
Department of Obstetrics and Gynecology, Baylor College of Medicine, Houston, Texas USA
Address correspondence to Rodrigo Ruano, MD, PhD, Pavilion for Women, Texas Children's Fetal Center, 6651 Main St, Suite F1020, Houston, TX 77030 USA.Search for more papers by this authorAbstract
Objectives
The purpose of this study was to evaluate the impact of standardization of the lung-to-head ratio measurements in isolated congenital diaphragmatic hernia on prediction of neonatal outcomes and reproducibility.
Methods
We conducted a retrospective cohort study of 77 cases of isolated congenital diaphragmatic hernia managed in a single center between 2004 and 2012. We compared lung-to-head ratio measurements that were performed prospectively in our institution without standardization to standardized measurements performed according to a defined protocol.
Results
The standardized lung-to-head ratio measurements were statistically more accurate than the nonstandardized measurements for predicting neonatal mortality (area under the receiver operating characteristic curve, 0.85 versus 0.732; P = .003). After standardization, there were no statistical differences in accuracy between measurements regardless of whether we considered observed-to-expected values (P > .05). Standardization of the lung-to-head ratio did not improve prediction of the need for extracorporeal membrane oxygenation (P> .05). Both intraoperator and interoperator reproducibility were good for the standardized lung-to-head ratio (intraclass correlation coefficient, 0.98 [95% confidence interval, 0.97–0.99]; bias, 0.02 [limits of agreement, −0.11 to +0.15], respectively).
Conclusions
Standardization of lung-to-head ratio measurements improves prediction of neonatal outcomes. Further studies are needed to confirm these results and to assess the utility of standardization of other prognostic parameters.
References
- 1Cannie MM, Jani JC, De Keyzer F, Allegaert K, Dymarkowski S, Deprest J. Evidence and patterns in lung response after fetal tracheal occlusion: clinical controlled study. Radiology 2009; 252: 526–533.
- 2Gucciardo L, Deprest J, Done E. Prediction of outcome in isolated congenital diaphragmatic hernia and its consequences for fetal therapy. Best Pract Res Clin Obstet Gynaecol 2008; 22: 123–138.
- 3Langham MRJr, Kays DW, Ledbetter DJ, Frentzen B, Sanford LL, Richards DS. Congenital diaphragmatic hernia: epidemiology and outcome. Clin Perinatol 1996; 23: 671–688.
- 4Jani JC, Benachi A, Nicolaides KH. Prenatal prediction of neonatal morbidity in survivors with congenital diaphragmatic hernia: a multicenter study. Ultrasound Obstet Gynecol 2009; 33: 64–69.
- 5Ruano R, Aubry MC, Barthe B, Mitanchez D, Dumez Y, Benachi A. Predicting perinatal outcome in isolated congenital diaphragmatic hernia using fetal pulmonary artery diameters. J Pediatr Surg 2008; 43: 606–611.
- 6Jani JC, Nicolaides KH, Gratacos E. Severe diaphragmatic hernia treated by fetal endoscopic tracheal occlusion. Ultrasound Obstet Gynecol 2009; 34: 304–310.
- 7Peralta CF, Jani JC, Van Schoubroeck D, Nicolaides KH, Deprest JA. Fetal lung volume after endoscopic tracheal occlusion in the prediction of postnatal outcome. Am J Obstet Gynecol 2008; 198: 60.e1–60.e5.
- 8Ruano R, da Silva MM, Campos JA. Fetal pulmonary response after fetoscopic tracheal occlusion for severe isolated congenital diaphragmatic hernia. Obstet Gynecol 2012; 119: 93–101.
- 9Ruano R, Duarte SA, Pimenta EJ. Comparison between fetal endoscopic tracheal occlusion using a 1.0-mm fetoscope and prenatal expectant management in severe congenital diaphragmatic hernia. Fetal Diagn Ther 2011; 29: 64–70.
- 10Metkus AP, Filly RA, Stringer MD, Harrison MR, Adzick NS. Sonographic predictors of survival in fetal diaphragmatic hernia. J Pediatr Surg 1996; 31: 148–152.
- 11Arkovitz MS, Russo M, Devine P, Budhorick N, Stolar CJ. Fetal lung-head ratio is not related to outcome for antenatal diagnosed congenital diaphragmatic hernia. J Pediatr Surg 2007; 42: 107–111.
- 12Laudy JA, Van Gucht M, Van Dooren MF, Wladimiroff JW, Tibboel D. 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.
- 13Lipshutz GS, Albanese CT, Feldstein VA. Prospective analysis of lung-to-head ratio predicts survival for patients with prenatally diagnosed congenital diaphragmatic hernia. J Pediatr Surg 1997; 32: 1634–1636.
- 14Jani JC, Peralta CF, Nicolaides KH. Lung-to-head ratio: a need to unify the technique. Ultrasound Obstet Gynecol 2012; 39: 2–6.
- 15Peralta CF, Cavoretto P, Csapo B, Vandecruys H, Nicolaides KH. Assessment of lung area in normal fetuses at 12–32 weeks. Ultrasound Obstet Gynecol 2005; 26: 718–724.
- 16Britto IS, Araujo Júnior E, Sangi-Haghpeykar H. Reference ranges for 2-dimensional sonographic lung measurements in healthy fetuses: a longitudinal study. J Ultrasound Med 2014; 33: 1917–1923.
- 17Lazar DA, Cass DL, Rodriguez MA. Impact of prenatal evaluation and protocol-based perinatal management on congenital diaphragmatic hernia outcomes. J Pediatr Surg 2011; 46: 808–813.
- 18DeLong ER, DeLong DM, Clarke-Pearson DL. Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics 1988; 44: 837–845.
- 19Hanley JA, McNeil BJ. A method of comparing the areas under receiver operating characteristic curves derived from the same cases. Radiology 1983; 148: 839–843.
- 20McNeil BJ, Hanley JA, Funkenstein HH, Wallman J. Paired receiver operating characteristic curves and the effect of history on radiographic interpretation: CT of the head as a case study. Radiology 1983; 149: 75–77.
- 21Ruano R, Lazar DA, Cass DL. Fetal lung volume and quantification of liver herniation by magnetic resonance imaging in isolated congenital diaphragmatic hernia. Ultrasound Obstet Gynecol 2014; 43: 662–669.
- 22Ruano R, Yoshisaki CT, da Silva MM. A randomized controlled trial of fetal endoscopic tracheal occlusion versus postnatal management of severe isolated congenital diaphragmatic hernia. Ultrasound Obstet Gynecol 2012; 39: 20–27.
- 23Ruano R, Takashi E, da Silva MM, Haeri S, Tannuri U, Zugaib M. Quantitative lung index, contralateral lung area, or lung-to-head ratio to predict the neonatal outcome in isolated congenital diaphragmatic hernia? J Ultrasound Med 2013; 32: 413–417.
- 24Victoria T, Bebbington MW, Danzer E. Use of magnetic resonance imaging in prenatal prognosis of the fetus with isolated left congenital diaphragmatic hernia. Prenat Diagn 2012; 32: 715–723.
- 25Kehl S, Kalk AL, Eckert S. Assessment of lung volume by 3-dimensional sonography and magnetic resonance imaging in fetuses with congenital diaphragmatic hernias. J Ultrasound Med 2011; 30: 1539–1545.
- 26Jani J, Nicolaides KH, Keller RL. Observed to expected lung area to head circumference ratio in the prediction of survival in fetuses with isolated diaphragmatic hernia. Ultrasound Obstet Gynecol 2007; 30: 67–71.
- 27Ruano R, Takashi E, da Silva MM, Campos JA, Tannuri U, Zugaib M. Prediction and probability of neonatal outcome in isolated congenital diaphragmatic hernia using multiple ultrasound parameters. Ultrasound Obstet Gynecol 2012; 39: 42–49.
- 28Ruano R, Britto IS, Sangi-Haghpeykar H. Longitudinal assessment of lung area measurements by two-dimensional ultrasound in fetuses with isolated left-sided congenital diaphragmatic hernia. Ultrasound Obstet Gynecol 2015; 45: 566–571.
- 29Ruano R, Joubin L, Sonigo P. 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.
- 30Ruano R, Aubry MC, Barthe B, Mitanchez D, Dumez Y, Benachi A. Quantitative analysis of fetal pulmonary vasculature by 3-dimensional power Doppler ultrasonography in isolated congenital diaphragmatic hernia. Am J Obstet Gynecol 2006; 195: 1720–1728.
- 31Cruz-Martinez R, Hernandez-Andrade E, Moreno-Alvarez O, Done E, Deprest J, Gratacos E. Prognostic value of pulmonary Doppler to predict response to tracheal occlusion in fetuses with congenital diaphragmatic hernia. Fetal Diagn Ther 2011; 29: 18–24.
- 32Mahieu-Caputo D, Aubry MC, El Sayed M, Joubin L, Thalabard JC, Dommergues M. Evaluation of fetal pulmonary vasculature by power Doppler imaging in congenital diaphragmatic hernia. J Ultrasound Med 2004; 23: 1011–1017.
- 33Jani JC, Cordier AG, Martinovic J. Antenatal ultrasound prediction of pulmonary hypoplasia in congenital diaphragmatic hernia: correlation with pathology. Ultrasound Obstet Gynecol 2011; 38: 344–349.