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DOI: 10.1148/radiol.2442061158
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(Radiology 2007;244:575-582.)
© RSNA, 2007

Obstetric Imaging

Lung Volumes in Fetuses with Congenital Diaphragmatic Hernia: Comparison of 3D US and MR Imaging Assessments1

Jacques C. Jani, MD, Mieke Cannie, MD, Cleisson F. A. Peralta, MD, PhD, Jan A. Deprest, MD, PhD, Kypros H. Nicolaides, MD, and Steven Dymarkowski, MD, PhD

1 From the Unit of Prenatal and Gynaecological Ultrasound and Fetal Therapy, Department of Obstetrics and Gynaecology (J.C.J., J.A.D.), and Department of Radiology (M.C., S.D.), University Hospital Gasthuisberg, 3000 Leuven, Belgium; and Fetal Medicine Centre, King's College Hospital Medical School, London, England (C.F.A.P., K.H.N.). Received July 5, 2006; revision requested September 1; revision received September 30; accepted November 1; final version accepted December 22. J.C.J. supported by a grant from the European Commission in its 5th Framework Programme (QLG1 CT2002 01632; EuroTwin2Twin). C.F.A.P. supported by a grant from the Fetal Medicine Foundation (Registered Charity 1037116). Address correspondence to J.A.D. (e-mail: Jan.Deprest{at}uz.kuleuven.ac.be).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 IMPLICATIONS FOR PATIENT CARE
 References
 
Purpose: To prospectively compare three-dimensional (3D) ultrasonography (US) and magnetic resonance (MR) imaging in the assessment of lung volumes in fetuses with congenital diaphragmatic hernia.

Materials and Methods: Informed consent was obtained for this ethics committee–approved study. Left and right lung volumes were measured by using the 30° virtual organ computer-aided analysis 3D US technique and a transverse multiplanar T2-weighted MR imaging technique in 43 fetuses with isolated congenital diaphragmatic hernia. Regression analysis was used to determine the significance of the association between the two methods.

Results: The 43 fetuses were assessed in a total of 78 examinations. Median gestational age at the examinations was 28 weeks (range, 18–38 weeks). In all examinations, it was possible to visualize and measure both the ipsilateral and the contralateral lungs with MR imaging. In contrast, with 3D US, the contralateral lung could be measured in all examinations, but the ipsilateral lung could be measured in only 44 (56%) examinations. For the contralateral lungs, there was a significant association between 3D US and MR imaging measurements (r = 0.86, P < .001). Although the mean lung volume measured with 3D US was 25% lower than that measured with MR imaging, the ratio of observed volume to expected normal mean volume for gestation was not significantly different between the two methods (3D US, 0.48; MR imaging, 0.52). In the 44 examinations in which the ipsilateral lung could be measured with both methods, 3D US volumes were not significantly different from MR imaging volumes, and the association was weaker (r = 0.39, P < .05) in the ipsilateral lungs than in the contralateral lungs.

Conclusion: For congenital diaphragmatic hernia, 3D US provides a reliable measurement of the contralateral but not the ipsilateral lung.

© RSNA, 2007


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 IMPLICATIONS FOR PATIENT CARE
 References
 
In congenital diaphragmatic hernia, chronic intrathoracic pulmonary compression by the herniated abdominal viscera prevents normal development of the lungs. Congenital diaphragmatic hernia is associated with a high postnatal mortality due to pulmonary hypoplasia and/or hypertension (1–5).

It has been shown that in congenital diaphragmatic hernia, the development of both lungs is impaired, but more so in the ipsilateral lung than in the contralateral lung (6). In infants who die after repair of congenital diaphragmatic hernia, quantitative analysis of the bronchi, arteries, and alveoli has also confirmed that all of these structures are reduced in both lungs, but the ipsilateral lung is more severely affected (7,8).

Currently, antenatal prediction of the likely outcome and consequent counseling of the parents concerning their options—continuing with the pregnancy, possibly undergoing intrauterine surgery, or terminating the pregnancy—are based on two-dimensional ultrasonographic (US) measurement of the ratio of lung area to head circumference (1,2,5). Recently, it has become possible to measure fetal lung volume with three-dimensional (3D) US and magnetic resonance (MR) imaging (9–16). Thus, the aim of our study was to prospectively compare 3D US and MR imaging in the assessment of lung volumes in fetuses with congenital diaphragmatic hernia.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 IMPLICATIONS FOR PATIENT CARE
 References
 
Study Subjects and Design
This prospective study was conducted at the Fetal Medicine Unit and Radiology Department of the University Hospitals Leuven. Inclusion criteria were singleton pregnancies in which the fetus had isolated congenital diaphragmatic hernia and normal karyotype. On the basis of our findings, the patients were offered postnatal care with or without prenatal therapy or termination of pregnancy. Forty-three pregnant women found to have isolated congenital diaphragmatic hernia between December 2003 and January 2006 qualified for this study, consented to participate in the study, and agreed to undergo both 3D US and MR imaging examinations within 6 hours of each other. Our study was approved by the ethics committee on clinical studies of the University Hospitals Leuven. Each fetus was assessed one to four times with both 3D US and MR imaging during the pregnancy.

3D US Examination
Between three and five 3D volumes of the fetal chest were acquired with transabdominal US (RAB 4-8L probe, Voluson 730 Expert; GE Medical Systems, Milwaukee, Wis), preferably in a transverse plane with respect to the fetus. The volumes with the best image quality and showing the least amount of bone attenuation were chosen for analysis. We preferably acquired the volumes when the fetus was not moving and was facing the transducer. All examinations were performed by a single operator (J.C.J.) with extensive experience (5 years at the start of the study) in prenatal 3D US and obstetrical US in general (10 years of experience).

The sweep angle was set at 50°–85°, depending on the gestational age. The VOCAL (virtual organ computer-aided analysis) technique was used to obtain a sequence of six sections of each lung around a fixed axis, from the apex to the base, each after a 30° rotation from the previous section (17). The contour of each lung was drawn manually in the six different rotation planes to obtain the 3D volume measurement (Fig 1). The starting plane of rotation for each lung included the biggest anteroposterior diameters. Each measurement was performed off-line after scanning by a single trained operator (C.F.A.P., 5 years of experience in prenatal 3D US at the start of the study) who was not aware of the MR imaging findings. The time required to perform these measurements ranged from 5 to 10 minutes. MR imaging was always performed after 3D US.


Figure 1
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  		Figure 1: Volume calculation of the contralateral lung (outlined) in a fetus with left-sided congenital diaphragmatic hernia at 26 weeks gestation obtained with the virtual organ computer-aided analysis technique. The top left parasagittal US image corresponds to the starting plane of rotation (plane A), and the lower right virtual organ image corresponds to the final lung volume. Top right and bottom left images are coronal and transverse US scans, respectively.

 
MR Imaging Examination
MR imaging was performed with a clinical 1.5-T whole-body unit (Magnetom Sonata; Siemens, Erlangen, Germany) with gradient switching capabilities of 25 mT/m in 300 microseconds. Maternal sedation was induced with flunitrazepam (0.5 mg) administered orally 30 minutes before MR imaging to reduce fetal movements and related motion artifacts. Patients were positioned in a left-lateral position to prevent supine hypotension syndrome, and a combined six-channel phased-array body and spine coil was positioned over the lower pelvic area. The MR imaging protocol consisted of T2-weighted half-Fourier single-shot fast spin-echo image acquisitions. The standard geometric parameters of this protocol consisted of 38 adjacent 4-mm-thick sections, no intersection gap, a field of view of 380 x 380 mm, a matrix of 173 x 256, an echo time of 88 msec, a partial Fourier factor of 5/8, a resulting pixel resolution of 1.8 x 1.5 x 4.0 mm3, and a bandwidth of 475 Hz per pixel (18). These images were obtained by using intrinsic orthogonal transverse, coronal, and sagittal fetal body planes. No breath hold was requested.

The radiologist (M.C., 2 years of experience in fetal MR imaging at the start of the study) adjusted the number of sections and the image orientation during image acquisition for each fetus in a transverse plane, as required for optimal measurements of lung volumes (19). Sequences that were degraded by fetal motion were repeated. The mean (± standard deviation) examination time was 15 minutes ± 5.

In all 78 examinations, the side of the congenital diaphragmatic hernia, as well as the intrathoracic position of the liver, was noted with US and confirmed with MR imaging.

MR Imaging Planimetry
Planimetric measurements of lung volumes were performed by one author (M.C.). Lung volumes were calculated in the transverse plane by using sequences that allowed complete imaging of both lungs without motion-induced artifacts. The corresponding areas of each lung were determined on each section by using free-form regions of interest on a picture archiving and communication system (Impax; Agfa-Gevaert, Mortsel, Belgium). Measured areas were added and then multiplied by the section thickness to determine the entire volumes of the right and left lungs (Fig 2). The time required to perform these measurements ranged from 10 to 15 minutes. The author who performed these measurements was blinded to the 3D US findings.


Figure 2A
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  		Figure 2a: Transverse T2-weighted MR images (echo time, 88 msec; section thickness, 4 mm; field of view, 300 x 300 mm; matrix, 173 x 256) obtained at the thoracic level of a left-sided congenital diaphragmatic hernia in a fetus at 29 weeks gestation. (a) The spine is at the 6 o'clock position. There is a shift of the heart (H) and herniation of the small bowels (B), colon (C), stomach (S), and liver (L) through the defect. Note the positions of the spleen (Sp) and aorta (Ao). (b) Same transverse view with delineation of left (LL) and right (RL) lungs.

 

Figure 2B
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  		Figure 2b: Transverse T2-weighted MR images (echo time, 88 msec; section thickness, 4 mm; field of view, 300 x 300 mm; matrix, 173 x 256) obtained at the thoracic level of a left-sided congenital diaphragmatic hernia in a fetus at 29 weeks gestation. (a) The spine is at the 6 o'clock position. There is a shift of the heart (H) and herniation of the small bowels (B), colon (C), stomach (S), and liver (L) through the defect. Note the positions of the spleen (Sp) and aorta (Ao). (b) Same transverse view with delineation of left (LL) and right (RL) lungs.

 
Intraobserver Variability
For the assessment of the intraobserver variability of both methods, 30 fetuses were randomly chosen among the 43 patients included in the study. The repeated readings were separated by at least a 1-month interval.

Data and Statistical Analyses
Intraobserver variability for both 3D US (C.F.A.P.) and MR imaging (M.C.) was assessed for ipsilateral and contralateral fetal lung volumes in the same group of 30 fetuses by using intraclass correlation coefficients. Proportionate Bland and Altman analysis was performed to determine the agreement between the two methods. Bias was defined as the difference between the two methods, and limits of agreement were defined as 1.96 times the standard deviation of the mean difference (20).

The paired or nonpaired Student t test was used for comparison of normally distributed data, and the Mann-Whitney U or the Wilcoxon test was used for non–normally distributed data. Linear regression analysis with least-squares optimization was performed to determine the significance of the association between the two methods.

The difference in lung volume assessed with 3D US versus that assessed with MR imaging was defined as [(A – B)·100]/A, where A and B are the lung volumes obtained, respectively, with MR imaging and 3D US. Univariate regression analysis was used to investigate the effect on the difference in lung volume assessed with 3D US versus with MR imaging (in milliliters) of the measurement obtained with MR imaging as a continuous numerical variable and with side of congenital diaphragmatic hernia (left or right) and presence of intrathoracic herniation of the liver (yes or no) as categorical variables.

On the basis of previously established normative curves with the same method for lung volume measurement at 3D US and MR imaging, as performed in our study, the ratio of observed to expected fetal lung volume was calculated (12,14).

Statistical analysis was performed with Statistica 6.0 (StatSoft, Tulsa, Okla); SPSS for Windows, version 13 (SPSS, Chicago, Ill); and Excel, version 9.0 (Microsoft, Seattle, Wash). A P value of less than .05 was considered to represent a statistically significant difference.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 ADVANCES IN KNOWLEDGE
 IMPLICATIONS FOR PATIENT CARE
 References
 
Characteristics of the Population
There were 35 fetuses with left-sided congenital diaphragmatic hernia and eight with right-sided congenital diaphragmatic hernia. Together they accounted for a total of 67 and 11 examinations, respectively, with 3D US and MR imaging. The median gestational age was 28 weeks (range, 18–38 weeks). Intrathoracic herniation of the liver was observed in 38 fetuses and in 66 examinations. In all 78 examinations, it was possible to visualize and measure both the ipsilateral and the contralateral lungs with MR imaging. In contrast, with 3D US, it was possible to examine the contralateral lung in all examinations, but the ipsilateral lung could be examined in only 56% (n = 44) of the examinations.

Intraobserver Agreement
For intraobserver agreement regarding measurements of ipsilateral fetal lung volume with 3D US when the lung could be visualized (13 lungs), the intraclass correlation coefficient was 0.71 (P < .01). For the contralateral lung (n = 30), the correlation coefficient was 0.93 (P < .001). For intraobserver agreement regarding measurements of ipsilateral and contralateral fetal lung volume with MR imaging, intraclass correlation coefficients were 0.92 (P < .001) and 0.94 (P < .001), respectively. When only the fetuses in which 3D US of the ipsilateral lung yielded a result (13 lungs) were considered, the correlation coefficient was 0.95 (P < .001).

Contralateral Lungs
The mean contralateral fetal lung volume measured with 3D US was 25% lower than that measured with MR imaging (P < .001) (Table). There was a significant association between 3D US and MR imaging measurements (r = 0.86, P < .001) (Fig 3). The difference in lung volume measured with the two techniques was independent of lung size measured with MR imaging, side of congenital diaphragmatic hernia, and presence of intrathoracic herniation of the liver. The mean ratio of observed to expected fetal lung volume for the contralateral lung was not significantly different between 3D US and MR imaging (0.48 and 0.52, respectively; P > .05).


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  		Lung Volumes Measured with 3D US and MR Imaging

 

Figure 3
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  		Figure 3: Scatterplot depicts the correlation between measurements of contralateral lung volume (in milliliters) obtained with 3D US and MR imaging in 78 examinations of fetuses with congenital diaphragmatic hernia. The solid line is the regression line, and the dotted line is the line of equality.

 
The results regarding proportionate differences between the two measurements against their mean (95% limits of agreement) were displayed by using Bland and Altman analysis. Bias was 36%, and proportionate limits of agreement were –32% and +103% (Fig 4).


Figure 4
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  		Figure 4: Scatterplot generated by using the Bland and Altman method depicts the proportionate difference between the US and MR measurements against their mean. The solid line represents the proportionate mean difference. The dotted lines represent the 95% limits of agreement.

 
Ipsilateral Lungs
The mean ipsilateral fetal lung volume measured with 3D US was 37% lower than that measured with MR imaging (P < .001) (Table). However, when only those examinations in which the lung was visible at 3D US were considered, there was no significant difference in mean lung volume measurements between the two techniques (Table). The 34 examinations (44%) in which the ipsilateral lungs could not be adequately visualized with 3D US tended to be limited to the smallest lung range; in 30 of these examinations (88%), the ipsilateral lung volume at MR imaging was less than 5 mL (Fig 5). The mean ipsilateral lung volume measured with MR imaging was smaller in examinations in which 3D US did not yield a result than in examinations in which 3D US yielded a result (P < .05) (Table).


Figure 5
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  		Figure 5: Scatterplot depicts the correlation between measurements of ipsilateral lung volume (in milliliters) obtained with 3D US and MR imaging in 78 examinations of fetuses with congenital diaphragmatic hernia. The solid line is the regression line based on measurements in which both methods yielded a result (n = 44). The dotted line is the line of equality.

 
In the 44 examinations in which both methods yielded a result, linear regression analysis revealed a poorer association between 3D US and MR imaging (r = 0.39, P < .05) (Fig 5) as compared with findings in the contralateral lungs.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
ADVANCES IN KNOWLEDGE
 IMPLICATIONS FOR PATIENT CARE
 References
 
Our data demonstrate that in fetuses with congenital diaphragmatic hernia, there is good correlation between lung volume measurements obtained with 3D US and those obtained with MR imaging for the contralateral lung but much poorer correlation for the ipsilateral lung. For the contralateral lung, 3D US yielded an estimate of lung volume that was 25% lower than that estimated with MR imaging; this difference was independent of lung size, side of congenital diaphragmatic hernia, and presence of intrathoracic herniation of the liver. For the ipsilateral lung, 3D US did not yield a result in nearly 45% of examinations; in about 90% of these cases, the lung volume measured with MR imaging was less than 5 mL. The data also indicate that the reproducibility of lung volume measurements obtained with MR imaging was high for both lungs, but with 3D US, reproducibility was good for the contralateral lung only.

Investigators in two previous studies compared 3D US with MR imaging for the assessment of fetal lungs. The first group (21) examined 11 fetuses with congenital diaphragmatic hernia at 28–37 weeks gestation, with a median delay between the two examinations of 2 days (range, 0–6 days). They reported good agreement between the two methods for both the ipsilateral and the contralateral lungs (21). With 3D US, it was not possible to measure the ipsilateral lung in 36% of fetuses; with MR imaging, measurement was not possible in 45% of fetuses. The intraclass correlation coefficient for agreement between the two methods was 0.94, with no outliers detected on the Bland and Altman plot.

Investigators in the second study examined 22 fetuses at high risk for pulmonary hypoplasia at 18–37 weeks gestation, with MR imaging performed immediately after 3D US (22). The investigators reported that the mean total lung volume measured with 3D US was 28% lower than that measured with MR imaging. The width of the 95% confidence interval of the differences between both methods was also large (–54.90 mL, 31.44 mL) (22).

Investigators in several studies have reported normal ranges of lung volumes with gestation by using 3D US (9–12) or MR imaging (13–16), and the values obtained with 3D US have been consistently lower than those obtained with MR imaging (Fig 6). Furthermore, Peralta et al previously found that the underestimation of lung volumes measured with 3D US was more pronounced in abnormal lungs than in normal lungs (22).


Figure 6
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  		Figure 6: Graph depicts comparison of results among the most recent studies in which total lung volume with gestation was reported. For the MR imaging regression curves, the studies of Rypens et al (14) and Mahieu-Caputo et al (13) were used. For the regression curves obtained for 3D US with the virtual organ computer-aided analysis technique, the studies of Ruano et al (10) and Peralta et al (12) were used. For the regression curves obtained for two-dimension–based, 3D US re-evaluated volume calculation, the study of Moeglin et al (11) was used.

 
In vitro accuracy studies have revealed underestimation of (23) or good agreement (24) regarding the volume measurements obtained with 3D US as compared with the "actual" volumes. In vivo accuracy studies of lung volume measurements have revealed good agreement with findings at 3D US (25) and overestimation with MR imaging (19). In both studies, the actual in vivo lung volume was likely to be larger than that measured at postmortem examination in the nonperfused dehydrated lungs. A perfectly designed in vivo accuracy study of lung volume measurement is almost impossible to conduct. Therefore, the actual in vivo lung volume cannot be measured. On the basis of the above experimental studies, the comparison between normal ranges of human lungs, and our study results, it appears that 3D US may yield an underestimation of the volume measured with MR imaging and that the actual in vivo volume, although not measurable, is more likely to be closer to the MR imaging measurement than to the 3D US measurement. However, to our knowledge this has not yet been proved in any previous studies and needs further investigation.

The smaller number of measurement sections obtained with 3D US compared with the number of sections obtained with MR imaging could partly account for the possible underestimation. With the 30° rotation step, six planes are always used for lung delineations; in contrast, with MR imaging, between eight and 22 planes (median, 16) are used for the contralateral lung, depending on the lung size (19). It is possible that the larger gaps between the planes at 3D US lead to the exclusion of lung areas, especially in more distorted lungs, such as those seen in congenital diaphragmatic hernia (22). The use of a transverse multiplanar measurement technique with MR imaging may also account for the more accurate result (19).

Our finding that the ipsilateral lung could not be adequately visualized in nearly 45% of examinations is compatible with the results of previously reported studies (6,21,22). We further showed in our study that the inability to visualize the ipsilateral lung was dependent on the lung size measured with MR imaging and that for the contralateral lung of similar size, all lungs could be visualized with 3D US. Therefore, lung size was not the only determinant for the inability to visualize the ipsilateral lung. Moreover, there was poor correlation between measurements of the ipsilateral lung with both techniques. The intraclass correlation coefficient was also smaller for 3D US than for MR imaging. A possible explanation for our findings could be that while acquiring the 3D volumes, we took more care to visualize the contralateral lung than to visualize the ipsilateral lung. Another explanation could be that the echogenicity of the abdominal content herniated into the chest, which can be similar to that of the lung, might have jeopardized the identification of the ipsilateral lung contour. Further studies are needed to elucidate these findings.

To evaluate the reliability of and compare the results for both measurement techniques, intraobserver variability was assessed for each lung by using intraclass correlation coefficients with both techniques in the same group of 30 fetuses. We found that both methods were equally reliable for measurement of the contralateral lung only.

A limitation of our study was that some fetuses were included more than once since 43 fetuses were assessed in 78 examinations. However, we believe that this issue does not invalidate the main conclusions. Another limitation was that we failed to include outcome as an end point to our study, primarily because our population was heterogeneous in terms of management options (termination of pregnancy, fetal therapy, or expectant management). However, the prediction of outcome was not the aim of our study, and a comparison of 3D US and MR imaging for the ability to help predict survival in fetuses with congenital diaphragmatic hernia is part of an ongoing multicenter study. A final limitation was that our study was not designed for assessment of interobserver agreement with both modalities; rather, it was designed for assessment of intraobserver agreement only. This should certainly be further investigated.

In conclusion, regarding intraobserver variabilities, our results demonstrate that in fetuses with congenital diaphragmatic hernia, 3D US does not enable reliable measurement of the ipsilateral lung volume. Although the contralateral lung volume can be reliably assessed with both 3D US and MR imaging, the measurements obtained with the two methods are not interchangeable. The deficit in lung volumes in our fetuses, when compared with the appropriate normal mean lung volume for gestation, was similar between the two methods. The extent to which lung volume measurements obtained with MR imaging may be superior to those obtained with 3D US in the prediction of outcome in fetuses with congenital diaphragmatic hernia remains to be determined.


   ADVANCES IN KNOWLEDGE
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
IMPLICATIONS FOR PATIENT CARE
 References
 


   IMPLICATIONS FOR PATIENT CARE
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 IMPLICATIONS FOR PATIENT CARE
References
 


   ACKNOWLEDGMENTS
 
We thank P. Lewi, PhD, for statistical advice.


   FOOTNOTES
 

Abbreviations: 3D = three-dimensional

Authors stated no financial relationship to disclose.

Author contributions: Guarantors of integrity of entire study, J.C.J., M.C., J.A.D., S.D.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, all authors; clinical studies, all authors; statistical analysis, J.C.J.; and manuscript editing, all authors


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 IMPLICATIONS FOR PATIENT CARE
 References
 

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M. M. Cannie, J. C. Jani, F. De Keyzer, K. Allegaert, S. Dymarkowski, and J. Deprest
Evidence and Patterns in Lung Response after Fetal Tracheal Occlusion: Clinical Controlled Study
Radiology, June 9, 2009; (2009) 2522081955.
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