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Obstetric Imaging |
1 From the Department of Surgery, Fetal Treatment Center (B.W.P., J.B.L., M.R.H., C.T.A.), and Department of Radiology (F.V.C., Y.L., A.Q., R.A.F.), University of California, San Francisco, 513 Parnassus Ave, Rm HSW 1601, San Francisco, CA 94143-0570. Received September 20, 2000; revision requested November 3; revision received November 30; accepted January 15, 2001. Supported by National Institutes of Health grant M01 RR01271 (C.T.A.) and the UCSF Pediatric Clinical Research Center. Address correspondence to C.T.A. (e-mail: albanesec@surgery.ucsf.edu).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Prenatal MR imaging was performed in 26 fetuses with unilateral congenital diaphragmatic hernia. Two independent observers performed planimetric measurement of lung volume. Relative lung volume was calculated as the observed total lung volume expressed as a percentage of the total lung volume predicted from fetal size. Relative lung volume was correlated with the ultrasonographic lung-head ratio in left-sided congenital diaphragmatic hernias evaluated before 27 weeks gestation (n = 21) and with pregnancy outcome in all cases of isolated left-sided congenital diaphragmatic hernia without prenatal intervention (n = 11).
RESULTS: Observers demonstrated excellent agreement in total lung volume measurements at MR imaging, with an intraclass correlation coefficient of 0.95. Relative lung volume was positively correlated with lung-head ratio (r = 0.78, P < .001). By using rank order analysis in the pregnancy outcome group, relative lung volume was predictive of prognosis (P < .05) when adjusted for gestational age at delivery and birth weight. Three of four fetuses with a relative lung volume of less than 40% died.
CONCLUSION: Interobserver agreement is high at MR lung volumetry, and its findings are predictive of outcome in fetuses with isolated left-sided congenital diaphragmatic hernia.
Index terms: Fetus, growth and development, 856.128, 856.8754 • Fetus, MR, 60.121412, 60.12144, 856.121412, 856.12144 • Fetus, respiratory system, 60.1496, 856.8758 • Fetus, US, 856.12983, 856.12989 • Hernia, diaphragmatic, 856.8754 • Magnetic resonance (MR), volume measurement, 60.12144, 856.12144 • Pregnancy, US, 856.12983, 856.1311
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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The major prognostic factors are the presence of associated structural or chromosomal anomalies, herniation of the liver into the thorax, and the lung-head ratio (LHR) (5–8). The LHR is the product of the orthogonal diameters of the right lung at the level of the cardiac atria divided by the head circumference (all measured in millimeters). The LHR was developed as a measure of pulmonary hypoplasia in left-sided CDH. Head circumference is used as a denominator to adjust for fetal size. Higher and lower values of LHR are predictive of survival and demise, respectively, in left-sided CDH (7,8). However, the LHR often is in the indeterminate middle range and is only an indirect measure of pulmonary volume.
Recent advances in magnetic resonance (MR) imaging, particularly the development of single-shot rapid acquisition and relaxation enhancement, make it possible to routinely obtain high-quality T2-weighted images of the fetus during maternal breath holding, without fetal sedation (9,10). Fetal volumetric measurements can be readily performed on MR images by using planimetry (11–13). A previous study (14) demonstrated the feasibility of using MR lung volumetry in fetuses with normal or hypoplastic lungs and showed that total lung volume in fetuses with normal lungs can be accurately predicted from biometric parameters related to fetal size. The relative fetal lung volume can be calculated by expressing the observed volume as a percentage of the lung volume predicted from biometric measurements.
The purpose of the present study was to determine the interobserver variability of prenatal MR lung volumetry and to assess the value of MR lung volumetric findings as predictors of outcome in fetuses with CDH.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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US Technique and Interpretation
All patients underwent contemporaneous routine US evaluation performed by one of four experienced sonologists (including R.A.F.) at our institution. US was performed with state-of-the-art equipment (Sequoia; Acuson, Mountain View, Calif) by using 3.5–8-MHz transducers and combined gray-scale and color Doppler examination. The LHR was measured in fetuses with left-sided CDH manifesting at 20–27 weeks gestation (n = 21) (8). The LHR was not measured in fetuses with right-sided CDH (n = 4) and in one fetus with left-sided CDH evaluated after 27 weeks gestation. The LHR is the product of the orthogonal diameters of the right lung at the level of the cardiac atria divided by the head circumference (all measured in millimeters). Liver position was determined by using color Doppler imaging of the hepatic vessels, as previously described (6).
MR Technique and Interpretation
MR imaging was performed with a 1.5-T superconducting magnet (Signa; GE Medical Systems, Milwaukee, Wis) and a four-element phased-array surface coil (GE Medical Systems). T1-weighted images were obtained by using a breath-hold spoiled gradient-echo sequence with a repetition time of 100–140 msec, an echo time of 4.2 msec, a flip angle of 70°–90°, a matrix of 256 x 128–192, and one signal acquired. T2-weighted images were obtained by using a single-shot rapid acquisition and relaxation enhancement sequence, with a repetition time of 100–140 msec, an effective echo time of 90 msec, and a matrix of 256 x 160–256. A minimal bandwidth was used for all sequences. Sequence acquisition times were all 15–30 seconds. Section thickness and intersection gap were 4–6 and 0–1 mm, respectively. The supervising radiologist (F.V.C.) optimized the field of view, number of sections, section thickness, and intersection gap to each individual patient. Images that were nondiagnostic due to fetal motion were repeated. T2-weighted images were obtained in transverse, sagittal, and coronal planes.
Two independent readers (F.V.C., A.Q.) performed planimetric measurements of lung volumes in all cases, as previously described (14). The readers were aware that the fetuses had CDH but were unaware of other clinical or US findings. Readers selected images acquired with the single-shot rapid acquisition and relaxation enhancement sequences that were used to completely image both lungs without motion or section misregistration artifacts. The cross-sectional area of the lung was measured on each section by using a picture archiving and communication system (Impax; Agfa-Gevaert, Leverkusen, Germany) free-form region-of-interest tool. The area was multiplied by the combination of section thickness and intersection gap to calculate the volume for that section. The volumes for all sections were then added to calculate the volume of the entire lung, and the final lung volume was obtained by averaging the volume measured on transverse, sagittal, and coronal images.
The calculation was repeated for the contralateral lung, and the volumes of both lungs were added to calculate the total lung volume. To quantify the degree of pulmonary hypoplasia, a relative lung volume was calculated by expressing the observed total lung volume as a percentage of the predicted total volume. Observed total lung volume was considered as the mean value of the measurements recorded by both readers. Predicted total lung volume was calculated by using the following equation based on biometric parameters of fetal size: Predicted total lung volume in milliliters = (0.47 x liver volume in milliliters) + (0.76 x biparietal diameter in millimeters) - (0.39 x femur length in millimeters) - 18.9.
This equation has been shown (14) to yield an accurate estimate of total lung volume in fetuses with normal lungs. The two readers had different levels of experience in MR fetal lung volumetry: The more experienced reader had performed more than 50 fetal MR lung volume measurements, whereas the less experienced reader had performed 10.
Outcome
For the evaluation of outcome, only fetuses without factors confounding fetal survival were considered. Fifteen fetuses were excluded from outcome analysis due to one or more of the following: termination of pregnancy (n = 3), fetal surgery (n = 9), right-sided CDH (n = 5), or other anomalies (n = 3). The observed anomalies included a facial cleft and congenital heart disease in one fetus, left cerebellar atrophy in one fetus, and a two-vessel cord and echogenic bowel in one fetus. Follow-up data collected prospectively consisted of whether the neonate was alive at the time of discharge from the hospital, need for extracorporeal membrane oxygenation, duration of mechanical ventilation, gestational age at delivery, and birth weight. All neonates were delivered at our institution or another tertiary care center. The mean gestational age at birth was 38.3 weeks (range, 33.3–40.6 weeks), and the mean birth weight was 2,883 g (range, 2,400–3,537 g).
Statistical Technique
The interobserver variability of MR imaging was assessed by using the intraclass correlation coefficient. All 26 fetuses were included in the assessment of interobserver variability. The 11 fetuses included in the outcome analysis were assigned a severity rank, where death was considered the worst outcome and the need for extracorporeal membrane oxygenation support and for mechanical ventilation were ranked as the second and third worst outcomes, respectively. Patients were substratified according to the time to demise or duration of ventilatory support. Outcome rank was numbered from 1 (worst) to 11 (best). Spearman correlation coefficients were used to measure the univariate association between radiologic measures and outcome severity rank. A linear model was used to evaluate the relationship between individual radiologic measure (LHR or relative lung volume) and severity rank. Adjustment was made for gestational age at delivery and birth weight, since these factors might have affected outcome and severity rank. Severity rank was the dependent variable in the regression analysis. Gestational age at delivery, birth weight, and radiologic measures were the independent variables. The use of the absolute value of the observed independent variables versus their rank in the regression analysis did not change the statistical significance.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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The second objective of our study was to determine the prognostic value of MR lung volumetric findings in fetuses with isolated left-sided CDH. We demonstrated that relative lung volume is significantly correlated with LHR in left-sided CDH. We examined this correlation because, to our knowledge, LHR is currently the only measurement of pulmonary hypoplasia that has been clinically proved to be predictive of outcome. The positive correlation between relative lung volume and LHR suggests that relative lung volume should also be predictive of outcome. We confirmed this by showing that relative lung volume was predictive of outcome severity rank in the subgroup of 11 neonates with isolated left-sided CDH who were delivered without prenatal intervention.
These findings suggest that relative lung volume is a valid measure of pulmonary hypoplasia. Relative lung volume is potentially preferable to LHR as a predictive parameter because it demonstrates high reproducibility and because the expression of lung volume as a percentage of the predicted value is an intuitive measurement that may facilitate interpretation by both clinicians and patients.
However, our study did not include enough cases to allow comparison of the predictive power of relative lung volume and LHR. Additional studies with larger patient numbers are required before relative lung volume can be incorporated into routine prenatal evaluation.
In contrast to our results, findings in a recent study (15) failed to demonstrate a correlation between lung volume measured prenatally with MR imaging and outcome for fetuses with CDH. In this study, both absolute lung volume and relative lung volume calculated as absolute lung volume divided by gestational age were used. However, fetal lung volume has been shown (14) to correlate more closely with fetal size than with gestational age. The use of predicted lung volume derived from fetal size as a denominator for relative lung volume, rather than gestational age, may explain why in our study relative lung volume was predictive of outcome.
The main limitation of our study is the small number of cases available for outcome analysis. As noted, this precluded comparison of the predictive value of LHR with relative lung volume. In addition, the small number of cases limited our ability to investigate the effect of variables other than lung volume on pregnancy outcome. These variables include clinical factors such as age at delivery, birth weight, and postnatal arterial blood gas values.
Another limitation is the lack of a pathologic standard of reference for the diagnosis and quantification of pulmonary hypoplasia. This is a general problem in prenatal imaging research because tissue diagnoses rarely are available. However, the high reproducibility of MR lung volumetry and the correlation with LHR are consistent with the true lung volume. A final limitation is the potential selection bias in the study. Patients who are examined at our institution are often interested in prenatal surgery, and this may have biased our referral base toward more severe cases of CDH.
In conclusion, fetal MR lung volumetry can be used to demonstrate minimal interobserver variability, and its findings are correlated with outcome in CDH; a relative lung volume of less than 40% suggests a poor postnatal outcome in fetuses with isolated left-sided CDH. However, the limited case number warrants a more comprehensive study to confirm these findings and to assess the comparative predictive value of relative lung volume versus LHR.
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FOOTNOTES |
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Author contributions: Guarantor of integrity of entire study, F.V.C.; study concepts, F.V.C., C.T.A., R.A.F.; study design, B.W.P., C.T.A.; literature research, B.W.P., F.V.C.; clinical studies, F.V.C., R.A.F.; data acquisition, F.V.C., A.Q.; data analysis/interpretation, J.B.L., F.V.C., R.A.F.; statistical analysis, Y.L.; manuscript preparation and definition of intellectual content, F.V.C., B.W.P.; manuscript editing, B.W.P., F.V.C., Y.L.; manuscript revision/review, M.R.H., C.T.A., R.A.F.; manuscript final version approval, R.A.F., C.T.A., F.V.C.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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) with isolated left-sided CDH who did not undergo prenatal intervention. Severity is ranked from 1 (worst outcome) to 11 (best outcome). Low relative lung volume is associated with a poorer outcome; three of four fetuses with a relative lung volume of less than 40% died.