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Obstetric Imaging |
1 From the Departments of Radiology (F.V.C., Y.L., H.H., R.A.F.) and Surgery (J.B.L., C.T.A., M.R.H.), Fetal Treatment Center, University of California San Francisco, 505 Parnassus Ave, Box 0628, L-308, San Francisco, CA 94143-0628. Received July 19; revision requested September 17; revision received October 11; accepted October 26. Address correspondence to F.V.C. (e-mail: Fergus.Coakley@radiology.ucsf.edu).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Single-shot rapid acquisition with relaxation enhancement (RARE) magnetic resonance (MR) imaging was used to perform planimetric measurement of total lung volume in 46 fetuses at 18–32 weeks gestation. Total lung volume was correlated with gestational age, and biometric parameters in fetuses were correlated with normal chest findings at ultrasonography (US) (n = 24). This analysis was used to evaluate relative lung volume in fetuses suspected of having pulmonary hypoplasia (n = 22).
RESULTS: Normal fetal total lung volume was strongly correlated with liver volume measured at MR imaging (r = 0.94), fetal weight estimated at US (r = 0.93), head circumference measured at US (r = 0.90), and gestational age (r = 0.87). In fetuses suspected of having pulmonary hypoplasia, the relative lung volume varied from 4.6% to 81.6% when the observed total lung volume was expressed as a percentage of the predicted total lung volume.
CONCLUSION: Normal fetal total lung volume is strongly correlated with biometric measurements. Relative fetal lung volume can be calculated by expressing the observed volume as a percentage of the predicted volume calculated from biometric measurements; knowledge of the relative fetal lung volume assists in the confirmation and quantification of fetal pulmonary hypoplasia.
Index terms: Fetus, growth and development, 856.128 • Fetus, MR, 60.121411, 60.121412, 856.121411 • Fetus, respiratory system, 60.141, 856.8758 • Fetus, US, 856.12981, 856.12983 • Hernia, diaphragmatic, 856.8754 • Magnetic resonance, volume measurement
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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A variety of ultrasonographic (US) features have been analyzed as prognostic indicators in CDH (7–13). US evaluation of pulmonary hypoplasia is limited by poor acoustic differentiation of ipsilateral fetal lung tissue from surrounding structures (7,8). This limitation also applies to volumetric measurement with three-dimensional US (14). At magnetic resonance (MR) imaging, the fetal lungs are well depicted because they have high signal intensity on T2-weighted images (15) presumably because, in utero, they are filled with amniotic fluid and not air.
The recent development of the single-shot rapid acquisition with relaxation enhancement (RARE) sequence, a rapid spin-echo–based T2-weighted sequence, has been a major advance in fetal MR imaging (15). Single-shot RARE has a section acquisition time of less than a second that essentially "freezes" fetal motion and makes it possible to routinely obtain high-quality T2-weighted images of the fetus during maternal breath holding without fetal sedation (16–18). Single-shot RARE sequences are commercially available as single-shot fast spin-echo (SSFSE; GE Medical Systems, Milwaukee, Wis) and half-Fourier acquisition single-shot turbo spin-echo (HASTE; Siemens, Erlangen, Germany) sequences.
Fetal volumetric measurements can be readily performed on MR images with planimetry (19–21). In published studies (19–21), normal lung volume has been related to gestational age rather than fetal biometric measurements, but lung volume in fetuses suspected of having pulmonary hypoplasia was not assessed. For these reasons, we undertook this study to determine which biometric parameters are most closely correlated with normal fetal total lung volume and to investigate the feasibility of using these parameters to evaluate fetal pulmonary hypoplasia.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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There were 54 singleton and three twin pregnancies, so a total of 60 fetuses were evaluated. Fifty-five fetuses met the single inclusion criterion, a gestational age of 18–32 weeks. A detailed obstetric US examination had been performed at our institution in all of these 55 fetuses. Five of these 55 fetuses were excluded because the lungs were not completely included on the MR images. (The lungs were not routinely included in the field of view. Our study was performed retrospectively and included cases in which the chest was not the area of clinical concern.) Four fetuses were excluded because of US abnormalities that could likely confound fetal biometry or MR lung volumetry, namely, cranial enlargement due to hydrocephalus (n = 2) and pleural effusions associated with hydrops fetalis (n = 2). The remaining 46 fetuses in 44 patients formed the study group.
The mean maternal age in the study group was 32 years (age range, 14–42 years), and the mean gestational age was 24 weeks. On the basis of the US results, fetuses were classified as having a normal chest (n = 24) or conditions associated with pulmonary hypoplasia (n = 22). The latter consisted of CDH (n = 19), thoraco-omphalopagus (n = 2), and severe oligohydramnios (n = 1). Indications for MR imaging in the 24 fetuses with normal lungs were isolated lateral cerebral ventriculomegaly (n = 9), low-grade intracranial hemorrhage (n = 4), spinal anomaly (n = 4), Dandy-Walker syndrome (n = 3), amniotic band syndrome (n = 1), suspected placenta accreta (n = 1), suspected tuberous sclerosis (n = 1), and suspected small cranial meningocele (n = 1). None of these US neurologic abnormalities was associated with cranial enlargement.
US Technique and Interpretation
All patients underwent a detailed obstetric US evaluation at our institution. US was performed by using state-of-the-art equipment (Sequoia; Acuson, Mountain View, Calif) with 3.5–5.0-MHz transducers and combined gray-scale and color Doppler examinations. All US studies were reviewed and reported by one of several attending radiologists (including R.A.F.) with extensive experience in prenatal US. US biometric measurements were recorded for correlation with fetal lung volumes. Biometric measurements included estimated fetal weight, biparietal diameter, femur length, and head circumference.
The diagnosis of unilateral CDH (18 of 22 fetuses), the most common condition in the group of fetuses suspected of having pulmonary hypoplasia, was established by identifying herniated abdominal viscera in the fetal chest with associated mediastinal shift. In left-sided CDH, the herniated viscera typically consisted of the stomach, liver, and bowel. In right-sided CDH, the herniated viscera typically consisted of the liver, gallbladder, and bowel. Pulmonary hypoplasia in unilateral CDH was estimated at US by use of a measurement known as the lung-head ratio (LHR) (8). This measurement is used to assess the relative size of the contralateral lung by expressing the lung cross-sectional area measured at the level of the cardiac atria (in square millimeters) as a ratio of the head circumference (in millimeters). To our knowledge, no US biometric evaluation of the ipsilateral lung is possible in CDH. No US measurements of lung size were performed in the twins with thoraco-omphalopagus, in the fetus with bilateral CDH, or in the fetus with severe oligohydramnios.
MR Imaging Technique and Image Interpretation
MR imaging was performed on the same day as US in 27 fetuses, within 1–4 days in 10 fetuses, and after 9–22 days in seven fetuses. MR imaging was performed with a 1.5-T superconducting magnet (Signa; GE Medical Systems) 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 msec/echo time msec of 100–150/4.2, a flip angle of 70°–90°, a 256 x 128–192 matrix, and one signal acquired. T2-weighted images were obtained by using a single-shot RARE sequence (
/90 [effective]) with a 256 x 160–256 matrix.
A variable bandwidth was used with all sequences. Sequence acquisition time was 15–30 seconds. Section thickness and intersection gap were 4–6 mm and 0–1 mm, respectively. The supervising radiologist optimized the field of view, number of sections, section thickness, and intersection gap for each patient. Sequences that resulted in nondiagnostic images because of fetal motion were repeated; the technical parameters were altered when necessary to produce a shorter acquisition time. MR images were interpreted by attending radiologists who were experienced in MR imaging and who had a special interest in genitourinary radiology (F.V.C., H.H.). These radiologists generated only one interpretation for each study, either alone or by consensus.
Lung volume was calculated by selecting the single-shot RARE sequence that allowed complete imaging of both lungs (Fig 1) without motion or section misregistration artifact. The cross-sectional area of the lung was measured on each section by using a picture archiving and communications system, or PACS (Impax; Agfa-Gevaert, Mortsel, Belgium), free-form region-of-interest tool (Fig 2). The area was multiplied by the combination of section thickness and intersection gap to determine the volume for that section. The volumes for all sections were then added to determine the volume of the entire lung. The calculation was repeated for the contralateral lung, and the volumes of both lungs were combined to determine the total lung volume.
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On the basis of the analysis of fetuses with normal lungs, a stepwise linear regression formula that incorporated a combination of biometric parameters was devised to predict lung volume. This formula was used to calculate expected total lung volume in the fetuses suspected of having pulmonary hypoplasia at US. In fetuses in which all the necessary parameters were unavailable or unreliable (eg, liver volume in the conjoint twins with thoraco-omphalopagus and a fused liver), the expected lung volume was calculated from the regression formula for estimated fetal weight (n = 4) or head circumference (n = 2). We expressed the observed total lung volume as a percentage of the expected total volume to quantitate the degree of pulmonary hypoplasia. The resultant relative lung volume was correlated with the LHR in the 18 fetuses with unilateral CDH.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The relationship between observed and predicted lung volume in both fetuses with normal lungs and fetuses suspected of having pulmonary hypoplasia is illustrated in Figure 6. In fetuses with unilateral CDH, the relative degree of pulmonary hypoplasia ranged from 8.4% to 41.4% (mean, 28.6%). There was a positive correlation between the relative lung volume and LHR in the 18 fetuses with unilateral CDH (r = 0.50, P < .05).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Our results show that, at midgestation, normal total fetal lung volume is strongly correlated with gestational age and biometric indices of fetal size; the correlation is stronger for biometric parameters than for gestational age. These results confirm the intuitive concept that lung size should be more closely related to fetal size than fetal age and indicate that factors other than fetal size appear to have little influence on fetal lung volume. This strong correlation also implies that findings at fetal lung MR volumetry are meaningful and consistent in this gestational period.
The second objective of our study was to investigate the feasibility of using the correlation between normal total lung volume and biometric data to confirm and quantitate pulmonary hypoplasia in fetuses with abnormal lungs. We calculated the expected lung volume in 22 fetuses suspected of having pulmonary hypoplasia at US and then quantitated the degree of pulmonary hypoplasia by expressing the observed total lung volume as a percentage of the expected lung volume. Smaller-than-expected lung volumes were found in all 22 fetuses; relative lung volumes ranged from 4.6% to 81.6%. Of note, three fetuses had conditions associated with pulmonary hypoplasia at US (thoraco-omphalopagus in conjoint twins and severe oligohydramnios in one fetus), but the possibility of pulmonary hypoplasia was not raised until after lung MR volumetry was performed.
These results suggest that MR volumetry can be used in the evaluation of fetal pulmonary hypoplasia. Our results add to those of other studies of prenatal lung volume assessment. We have demonstrated a correlation with gestational age (r = 0.87) that is slightly higher than that of previous investigators (r = 0.80–0.88 [19,21]) probably because we excluded fetuses beyond 32 weeks gestation, when lung volume becomes more variable (21). In addition, we have shown that lung volume is more closely related to fetal size than to gestational age.
To our knowledge, the use of MR imaging to confirm and quantitate fetal pulmonary hypoplasia has not been previously described, although US has been used in the evaluation of pulmonary hypoplasia in CDH. In a logistic regression analysis of the prognostic value of prenatal US in isolated left CDH, the LHR was the only factor that was independently predictive of survival (13). The LHR was designed as an indirect indicator of pulmonary hypoplasia, with head circumference used as a denominator to adjust for differences in gestational age. The correlation between the LHR and relative lung volume in the 18 fetuses with unilateral CDH suggests that both the LHR and lung volumes obtained at MR imaging can be used to assess pulmonary hypoplasia.
It remains to be seen whether relative lung volume will be a stronger prognostic indicator than LHR obtained at US, although, in theory, MR volumetric findings have several potential advantages over LHR. MR volumetry is used to measure total lung volume rather than cross-sectional area. MR volumetry can be used in conditions other than CDH. MR volumetry allows expression of pulmonary hypoplasia as a percentage of the expected lung volume. The use of the relative lung volume percentage is advantageous because, while it requires the computation of more than a simple ratio, it can be derived from any of several biometric parameters (Table) and provides a common mode of expression that clinicians can readily understand.
Our study has several limitations. First, we did not have a histopathologic standard of reference for the diagnosis and quantification of pulmonary hypoplasia. This is a general problem in prenatal imaging research because histologic diagnoses are rarely available. However, pulmonary hypoplasia was a credible diagnosis in all 22 fetuses with abnormally low lung volumes, given the US diagnoses of CDH (n = 19), thoraco-omphalopagus (n = 2), and severe oligohydramnios (n = 1).
Second, we did not correlate the degree of pulmonary hypoplasia with clinical outcome. The primary aim of the study was to establish the feasibility of MR lung volumetry in fetuses with pulmonary hypoplasia, and we currently have insufficient data to perform an outcome analysis.
Third, our results for normal total fetal lung volume were derived from abnormal fetuses, who were undergoing MR imaging because they were suspected of having a variety of abnormalities at clinical or US examination. We believe that this method was reasonable because all of the control fetuses had normal chest findings at US and had diagnoses not known to be associated with pulmonary hypoplasia. Also, we did not include fetuses with an abnormality that might confound fetal biometry.
Fourth, a single observer performed all MR volumetric measurements without an analysis of intra- or interobserver variability. We used a single observer to minimize any learning-curve effect in the fetal MR imaging measurements. Such measurements had not been previously performed at our institution.
Fifth, we did not investigate possible changes in fetal lung volume related to the cardiac cycle or fetal breathing movements (14,19). Such changes would be extremely difficult to investigate since they would require monitoring of the fetal cardiac cycle and chest wall motion. It also seems likely that such changes would be small compared with the total lung volume measured at MR imaging, particularly when such changes are effectively averaged over the 15–30-second acquisition time of the single-shot RARE sequence.
Last, we have not defined a relative lung volume threshold for the diagnosis of pulmonary hypoplasia. We believe this is premature, given the novelty of our technique and the relatively small number of patients in our single-institution study. Nonetheless, the diagnosis of pulmonary hypoplasia should be strongly considered when the relative lung volume is below 80%–85% and when the clinical setting is appropriate.
In conclusion, normal fetal total lung volume measured at single-shot RARE MR volumetry is strongly correlated with biometric measurements related to fetal size; this correlation allows accurate prediction of fetal lung volume. Relative fetal lung volume can be calculated by expressing the observed lung volume measured at MR planimetry as a percentage of the predicted lung volume calculated from biometric measurements; knowledge of this volume assists in the confirmation and quantification of fetal pulmonary hypoplasia. Further research is required to establish the clinical utility and prognostic importance of these results.
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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., M.R.H.; study design, F.V.C., J.B.L.; definition of intellectual content, F.V.C.; literature research, F.V.C., J.B.L.; clinical studies, F.V.C., H.H., R.A.F.; data acquisition, F.V.C., R.A.F.; data analysis, F.V.C., Y.L.; statistical analysis, Y.L.; manuscript preparation and editing, F.V.C.; manuscript review, J.B.L., C.T.A., M.R.H., H.H., R.A.F.
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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) or pulmonary hypoplasia (
). Normal lung volume shows only slight individual variation from the predicted value on the basis of stepwise logistic regression analysis. Knowledge of this close correlation facilitates identification of pulmonary hypoplasia when lung volume is clearly less than the expected value.