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Published online before print December 29, 2003, 10.1148/radiol.2302021095
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(Radiology 2004;230:353-358.)
© RSNA, 2003

Experimental Studies

Fetal Sheep with Tracheal Occlusion: Monitoring Lung Development with MR Imaging and B-Mode US1

Ulrike Wedegaertner, MD, Mikhail Tchirikov, MD, Christian Habermann, MD, Kurt Hecher, MD, Jan Deprest, MD, Gerhard Adam, MD and Hobe J. Schroeder, MD

1 From the Departments of Diagnostic and Interventional Radiology (U.W., C.H., G.A.) and Gynecology (M.T., H.J.S.), University Hospital Hamburg Eppendorf, Martinistrasse 52, Hamburg 20246, Germany; AK Barmbek, Prenatal Medicine and Therapy, Hamburg, Germany (K.H.); and Department of Obstetric Gynecology, Hospital Gasthuisberg, Leuven, Belgium (J.D.). From the 2002 RSNA scientific assembly. Received September 1, 2002; revision requested November 4; final revision received April 10, 2003; accepted May 20. Address correspondence to U.W. (e-mail: wedegaer@uke.uni-hamburg.de).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To assess the accuracy of magnetic resonance (MR) imaging in determining fetal lung volume (FLV) and to observe fetal lung development with B-mode ultrasonography (US) and MR imaging.

MATERIALS AND METHODS: Seven sheep fetuses between 92 and 141 gestational days (term, 145 days) with and without tracheal occlusion (controls) underwent serial MR imaging and US. FLV at MR imaging was measured with true fast imaging with steady-state precession in coronal and transverse planes. The combined cross-sectional left- and right-lung area was measured with US at three transverse levels. FLV was measured at autopsy. Statistical evaluations included linear regression analysis and calculation of the mean and 95% CI.

RESULTS: No differences in FLV were observed on coronal or transverse MR images (r2 = 0.98; slope = 0.91; 95% CI: 0.82, 1.01). FLV at MR imaging at termination of the experiment was significantly related to FLV at autopsy (r2 = 0.96; slope = 1.27; 95% CI: 0.97, 1.57; n = 6). FLV at MR imaging increased more rapidly with gestational age in fetuses with tracheal occlusion (21.0 mL/d; 95% CI: 10.7, 31.3) than in controls (4.7 mL/d; 95% CI: 1.7, 7.7). Increase in left- and right-lung area at US was accelerated in fetuses with tracheal occlusion (1.60 cm2/d; 95% CI: 1.3, 1.9) compared with controls (0.38 cm2/d; 95% CI: 0.23, 0.53). Left- and right-lung area at US and FLV at MR imaging were significantly correlated (r2 = 0.82).

CONCLUSION: FLV can be measured with moderate accuracy at MR imaging on both coronal and transverse images. MR imaging and B-mode US are useful tools for monitoring and quantifying tracheal occlusion–stimulated fetal lung growth in sheep fetuses.

© RSNA, 2003

Index terms: Animals • Fetus, growth and development, 856.128, 856.8754, 856.8758 • Fetus, MR, 60.121416, 60.12144, 856.121416, 856.12144 • Fetus, US, 856.1298 • Hernia, diaphragmatic, 856.8754 • Trachea, stenosis or obstruction, 671.7522


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Congenital diaphragmatic hernia (CDH) is a fetal disorder with an incidence of one in 2,200 births per year (1). The mortality rate of 60% is caused predominantly by pulmonary hypoplasia and secondary pulmonary hypertension (2,3). The high mortality despite intensive perinatal care provides a compelling rationale for interventions that promote adequate fetal lung growth before birth. It is well established that prenatal tracheal occlusion leads to accelerated parenchymal lung growth in normal (4,5) and hypoplastic (4,6–8) lungs. Consequently, tracheal occlusion has been applied to selected human fetuses with severe CDH (9–11) to stimulate lung growth in utero and to improve survival rate after birth. It has not been established, however, how the effects of tracheal occlusion on lung growth can be monitored. After surgery, the effectiveness of tracheal occlusion—that is, the induction of pulmonary growth—has to be followed up and the possibility of overgrowth has to be checked. Therefore, an accurate and noninvasive imaging modality is needed. Both ultrasonography (US) and magnetic resonance (MR) imaging are noninvasive techniques that have recently been applied to human fetuses to depict the lung (12–18).

The purposes of our study were (a) to assess the accuracy of in vivo MR imaging in determining the fetal lung volume (FLV) by using lung volume at autopsy as the standard of reference and (b) to compare serial in vivo monitoring of the fetal lung development with B-mode US and with MR imaging. By using MR imaging, changes in lung volume with gestational age were observed, whereas with use of US, the development of cross-sectional lung areas at defined levels was examined.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
All experimental protocols were reviewed and approved by the local authorities on animal protection.

Subjects
MR imaging and US measurements were performed on seven ewes (Animal Care Facility of University Hospital Hamburg Eppendorf) with known conception dates carrying singleton fetuses at gestational ages ranging from 92 to 141 days (term, 145 days). In four sheep fetuses at 92–98 gestational days, the trachea was occluded during general anesthesia. The ewes were sedated with 0.25 mg per kilogram of body weight xylazine (Rompun; Bayer-Vital, Leverkusen, Germany), were intubated after intravenous administration of 1 g of barbiturate (Trapanal; Altana Pharma, Konstanz, Germany), and were anesthetized by means of artificial ventilation with 1% isoflurane (Forene; Abbot, Wiesbaden, Germany) with a 2:1 mixture of O2/N2O (O2, 2 L/min: N2O, 1 L/min). A short permanent catheter was inserted into the maternal external jugular vein. The maternal abdomen was incised in the midline, and the uterus was opened to exteriorize the fetal head and neck. The fetal trachea was exposed caudally from the larynx and was ligated with two ties. The fetal and maternal wounds were closed appropriately, and the animals recovered quickly. All surgical procedures were performed by M.T. and H.J.S.

Three fetuses without any surgical intervention served as controls. Because the effect of tracheal occlusion was used only as a tool to increase fetal lung growth, the control animals did not undergo sham operation.

B-Mode US
B-mode US was performed with state-of-the-art equipment (Aspen; Acuson, Mountain View, Calif) with 3.5–8.0-MHz transducers. US measurements of the fetal lung were performed after surgery at weekly intervals, if feasible, and 1 day before autopsy, with ewes placed in a lateral position by means of sedation (0.25 mg/kg xylazine). The fetal lung was visualized on-screen in transverse sections at three levels (level I, sinus vena porta; level II, apex of the heart; level III, a four-chamber view; Fig 1). All US scans were obtained by M.T.



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  		Figure 1. A four-chamber view (level III) from a B-mode US scan. Left- and right-lung areas were manually outlined as indicated for area determination.

 
MR Imaging
Animals were sedated with intravenously administered 20 mg diazepam (Ratiopharm, Ulm, Germany) and 250 mg (repeated as required) ketanest (Parke Davis, Karlsruhe, Germany) and then intubated. The inspired air was enriched with oxygen. All animals were examined in a lateral position with a phased-array body coil. MR imaging was performed with a 1.5-T imager (Magnetom Vision; Siemens, Erlangen, Germany) by using true fast imaging with steady-state precession sequences (4.8/2.3 [repetition time msec/echo time msec], 70° flip angle, 179 x 256 matrix, two acquisitions). Acquisition time was 12 seconds. Coronal and transverse images of the fetal thorax and abdomen were obtained. Section thickness and intersection gap were 5.0 and 1.5 mm, respectively. There were no fetal motion artifacts (with the exception of the heart) because of general anesthesia. MR imaging was performed in each fetus between 92 and 141 days of gestation at least on the day before autopsy and usually two to four times in intervals of 1–3 weeks. Images of diagnostic quality were obtained in all fetuses. FLVs were determined separately on transverse and coronal images (Fig 2a). MR measurements were performed by C.H. and U.W.



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  		Figure 2a. (a) Transverse and (b) coronal true fast imaging with steady-state precession MR images (4.8/2.3, 70° flip angle, 179 x 256 matrix, two acquisitions) obtained through fetal thorax 1 day before experiment termination in a fetus with tracheal occlusion at 128 gestational days. In a, note the outline of lung tracing. In b, rib impressions were also noted in the postmortem lungs (not shown) and are due to hyperplastic lung growth after tracheal occlusion.

 


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  		Figure 2b. (a) Transverse and (b) coronal true fast imaging with steady-state precession MR images (4.8/2.3, 70° flip angle, 179 x 256 matrix, two acquisitions) obtained through fetal thorax 1 day before experiment termination in a fetus with tracheal occlusion at 128 gestational days. In a, note the outline of lung tracing. In b, rib impressions were also noted in the postmortem lungs (not shown) and are due to hyperplastic lung growth after tracheal occlusion.

 
Lung Calculations
The investigators (M.T., U.W.) were not blinded because tracheal obstruction could be identified at MR imaging or US. MR and US studies were evaluated independently.

For US measurements, the surfaces of the left- and right-lung cross sections at each of the three levels were traced manually, and the respective areas (in square centimeters) were calculated by using the appropriate inherent function of the US device. For statistical evaluation, the areas of the left and right lung at each level were combined.

For volume determination at MR imaging, the area of the right and left lung was measured on each image with a free-form region-of-interest tool (Sienet MagicView VA31; Siemens) as follows: The lung tissue visible on each image was manually outlined (U.W.) as a region of interest (Fig 2a). The area of the region of interest was calculated by multiplying the number of pixels in the region of interest with the pixel size. The area of the region of interest was multiplied by the sum of the section thickness and intersection gap to determine the volume of the respective lung section. The volumes of all sections were then added to determine the volume of the entire lung. In each animal, we aimed to obtain the FLV from both transverse (FLVtrans) and coronal (FLVcor) images. To include the calculated lung volumes derived from both images, the FLV at MR imaging was calculated as (FLVcor + FLVtrans)/2, unless data from only one plane were available.

End of Experiments
The experimental protocol intended observation of the fetuses until close to term. However, whenever signs of imminent delivery became obvious, termination of the respective experiments had to be initiated; experiments thus varied from 20 to 44 days.

One day before the termination, US and MR examinations were performed. Experiments ended at 115–141 days of gestation by means of intravenous injection of an euthanasic solution (T61; Intervet International, Wiesbaden, Germany). Fetal body weight (towel dry) was determined at autopsy, and the completeness of tracheal occlusion was checked with the insertion of a thin probe into the trachea. Both lungs were removed, their volumes were measured by the displacement of isotonic saline, and lung weight was determined. Tracheal volume was calculated from the length and diameter of the trachea and was subtracted from the lung volume. The percentage of the relative lung weight was determined as lung weight-to-body weight ratio. Volume and weight calculations were performed by M.T. and H.J.S.

Statistical Evaluations
Average data are presented as means and 95% CIs. Linear regression analysis was performed to correlate FLV at MR imaging with postmortem lung weights, FLV at MR imaging and left- and right-lung areas at US with gestational age, FLVs in transverse with FLVs in coronal planes, and FLV at MR imaging with left- and right-lung areas at US performed within 1 day. Statistical and outlier analyses (Mahalanobis and Cook distance, deleted residual) were performed by using a commercial software package (Statistica; Statsoft, Tulsa, Okla). The difference in relative lung weights between fetuses with tracheal occlusion and controls was established with the Mann-Whitney test. P < .05 was considered to indicate a significant difference. The 95% prediction interval as a measure of accuracy was constructed with Statistica software package (19). For example (Fig 3), if FLV at MR imaging is determined to be 500 mL, the FLV at autopsy is with 95% probability between 270 and 415 mL.



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  		Figure 3. Graph shows 95% prediction interval (dashed lines) that reflects the accuracy of measuring FLVs at MR imaging (19). For example, if FLV at MR imaging is 500 mL, FLV at autopsy is with 95% probability between 270 and 415 mL. The outlier (fetus TO 2) is not included in calculation of the prediction interval. {bullet} = lung volume measurements of one animal at termination.

 

   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
There were 34 observations with B-mode US and 18 with MR imaging (Table 1). For practical reasons, the intended weekly observation intervals could not be followed in all cases, as indicated in Table 1. In one fetus with tracheal occlusion (fetus TO 7), the trachea was found to be incompletely closed at autopsy (inner diameter, 0.5–1.0 mm). Because there was no indication of stimulated lung growth, the fetus was regarded as a control. Thus, the control group consisted of four fetuses, and the tracheal occlusion group consisted of three fetuses. The relative lung weight in fetuses with tracheal occlusion (13.4%; 95% CI: 7.6, 19.3) was significantly larger (P <= .03) than that in controls (4.1%; 95% CI: 3.2, 4.9).


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  		TABLE 1. Gestational Age at Surgical Intervention and at Termination of the Experiment and Number of US and MR Observations

 
B-Mode US
Cross-sectional areas increased with gestational age (P < .02) at all three levels in controls and in fetuses with tracheal occlusion (Table 2, Fig 4), but with significantly steeper slopes in fetuses with tracheal occlusion.


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  		TABLE 2. Univariate Linear Regression Results of Areas and Gestational Age for All Levels at B-Mode US

 


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  		Figure 4. Graph shows an increase of cross-sectional lung area at level III with gestational age. Regression lines are given in Table 2. Cross-sectional areas increased with gestational age but with significantly steeper slopes in fetuses with tracheal occlusion ({blacksquare}) than in controls ({bullet}) at all three levels.

 
MR Imaging
FLVs on transverse and coronal images were highly correlated (r2 = 0.98; slope = 0.91; 95% CI: 0.82, 1.01; n = 13) and not different (Fig 2). In five of 18 observations, FLVs either on coronal (three observations) or transverse (two observations) images were used instead of the respective means. FLV measured at MR imaging 1 day before termination correlated well with the postmortem FLV (r2 = 0.84, n = 7). However, in one case (fetus TO 2), FLV at autopsy was 930 mL, whereas FLV at MR imaging was 750 mL. Because this measurement deviated (outlier evaluation) from the other six observations, it was omitted in calculating the linear regression between postmortem FLV (FLVP) and FLV at MR imaging (FLVMR): FLVMR = 63 + 1.27 · FLVp, where 1.27 is the slope of the regression line (95% CI: 0.97, 1.57); see Figure 3 (n = 6, r2 = 0.96). FLV at MR imaging increased more rapidly with gestational age in fetuses with tracheal occlusion than in controls (Fig 5). In fetuses with tracheal occlusion (seven observations), FLV at MR imaging increased 21.0 mL/d (95% CI: 10.7, 31.3); in controls (11 observations), the rate of increase was 4.7 mL/d (95% CI: 1.7, 7.7) and was significantly different from that in fetuses with tracheal occlusion.



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  		Figure 5. Graph shows increase of FLV at MR imaging with gestational age both in fetuses with tracheal occlusion ({blacksquare}) and in controls ({bullet}), with a more rapid increase in fetuses with tracheal occlusion. Linear regression lines for FLV at MR imaging in controls were -379 mL/d + 4.7 (95% CI: 1.7, 7.7) per gestational day and those in fetuses with tracheal occlusion were -1,979 mL/d + 21 (95% CI: 10.7, 31.3) per gestational day.

 
The cross-sectional areas measured at US were correlated with the FLV at MR imaging, when both were determined within 1 day. Left- and right-lung area at level III (as well as at levels I and II) and FLV at MR imaging were significantly correlated (r2 > 0.82, 14 observations), and an increase of 1 cm2 of left- and right-lung area at level III corresponded to a 12.5 mL (95% CI: 9.0, 16.0) increase of FLV at MR imaging.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
We found a high correlation between FLVs at MR imaging and postmortem FLVs (r2 = 0.84, n = 7), but the expected linear relationship was distorted for unknown reasons by the largest FLV value at MR imaging (fetus TO 2). With statistical considerations based on an outlier evaluation, we decided to omit this value from the linear regression analysis, which had increased the predictive value (r2 = 0.96, n = 6). One would expect FLVs at MR imaging to be larger than postmortem FLVs because lung dissection will reduce the liquid content (blood, lung fluid) of the lungs. This is supported somewhat by the slope of 1.27 of the regression line (Fig 3), though statistically it is not different from 1. The prediction interval in Figure 3 reveals that the accuracy of volume measurement is moderate. The width of the prediction interval is determined largely by the small number of animals used in this study, and a narrower range can be expected when more animals are investigated.

We have no explanation for the outlier value, but it is conspicuous that the largest lung shows this divergent result. Other volume and area measurements of this fetus (TO 2) at MR imaging are within the expected range. We assume that MR FLV measurements earlier in gestation also reflect the "true" FLV with a comparable accuracy, because most of the MR lung volumes determined at various gestational ages (Fig 5) are within the volume range covered in Figure 3.

Increase in lung volume with gestational age was observed in fetuses with tracheal occlusion and in controls at US and MR imaging alike. Lung growth was clearly accelerated in fetuses with tracheal occlusion and could be detected at both MR imaging and B-mode US. In one fetus (TO 7), MR and US monitoring did not demonstrate the expected accelerated lung growth after tracheal occlusion. The reason for the lack of growth stimulation became apparent at autopsy, which revealed an incomplete closure of the tracheal ligature, with normal relative lung weight. This fetus unintentionally simulates the failure of intrauterine tracheal occlusion at surgery and may be regarded as a negative control. This also demonstrates that the difficulty to blind the observers (M.H., U.W.) is of minor concern in our study, and it strongly supports the conclusion that MR imaging and US are reliable imaging modalities in monitoring in vivo lung growth after prenatal surgical interventions.

Accuracy of US and MR Imaging in Determining Lung Growth
MR imaging and US have been applied in several studies on human fetuses to investigate the clinical usefulness of the evaluation of FLVs (12–18). Duncan et al (15) studied the changes of normal FLV with increasing gestation and found an increase of lung volume from 8 to 125 mL during 20–40 weeks of gestation. In various studies (12,14,16,17,20,21), different MR imaging and US parameters were examined to quantify fetal pulmonary hypoplasia in CDH and to find prognostic factors to predict the outcome of CDH. However, little effort was made to investigate the accuracy of MR imaging and US in the determination of fetal lung growth and to directly compare both imaging techniques. The lack of knowledge of the "true" lung volume (at autopsy) was considered a general problem in prenatal imaging research because volume determinations are rarely available (17,18). Rypens et al (16) reported measurements of FLVs that were obtained in 11 human fetuses within 2 weeks following MR examination. In contrast to the results of our study, MR measurements of FLV by Rypens et al were 10% lower, which are probably due to the interval of up to 2 weeks between MR imaging and autopsy. In our study, MR measurements and lung volumes were obtained within 24 hours, which showed FLV at MR imaging to be close to the postmortem FLV.

Monitoring of Fetal Lung Growth
Monitoring of fetal lung development after tracheal occlusion is important to control the effects on lung growth, which range from no growth to aggressive growth with secondary hydrops. Variable lung growth responses to tracheal occlusion have been observed in early human trials (22,23). The absence of accelerated lung growth was due to incomplete tracheal closure, which was caused by, for example, small plugs or leaks in some cases (22,24). These observations correspond to our results, a failure of accelerated lung growth in one fetus with tracheal occlusion, with incomplete tracheal closure. If no accelerated lung growth is seen and the lung remains hypoplastic, it has to be taken into consideration whether tracheal occlusion has failed. In this case, reintervention probably has to be performed to obtain accelerated lung growth.

MR Imaging versus B-Mode US
According to our results, US and MR imaging are both suitable for determining fetal lung growth and are useful for monitoring fetal lung development. In comparison with US, MR imaging allows the determination of absolute lung volumes and offers excellent soft-tissue contrast, which is important in the separation of lung tissue from the surrounding structures such as the liver and mediastinum. On the other hand, US is widely available, less expensive, and less time consuming to perform. However, in cases of CDH and oligohydramnios, accurate visualization of the lung parenchyma is not always possible with US (15,25–28). In those cases, MR imaging seems to be advantageous for initial evaluations (15).

Several MR techniques have been used for FLV imaging, including single-shot rapid acquisition with relaxation enhancement, or RARE, (17), echo-planar MR imaging (15), half-Fourier RARE (14), and fast spin-echo T2-weighted imaging (16). We prefer true fast imaging with steady-state precession, which provides advantages such as short acquisition times and high fluid sensitivity, which offers an excellent contrast between the fluid-filled fetal lungs and the mediastinal and abdominal structures.

Limits of the Study
The main limitation of this study was the small number of sheep fetuses, which restricted the general validity of the results. Also, lack of fetuses with CDH had facilitated imaging, because determination of FLV in fetuses with liver herniation and pulmonary hypoplasia is expected to be more difficult. In this study, results were obtained from only healthy fetuses with and without tracheal occlusion, and it was not directly assessed whether MR imaging and US are useful in monitoring the stimulated growth of hypoplastic lungs.

Practical applications: We conclude that both B-mode US and MR imaging are useful tools for monitoring quantitatively fetal lung development in fetuses after prenatal tracheal occlusion. In comparison with US, MR imaging offers the advantage of measuring absolute lung volumes rather than lung areas and the imaging quality is superior in cases of oligohydramnios. However, US is less expensive and easier to perform than MR imaging. In this study, the relationship between cross-sectional lung areas and lung volumes at US has been quantified. In fetal sheep (last trimester), a 1-cm2 increase of the cross-sectional lung area at the level of the four-chamber view corresponds to a lung volume increase of 9–16 mL. To monitor fetal lung growth, we suggest an initial MR and US examination to determine the lung volume and the initial lung area and then follow-up lung volume growth by using B-mode US.


   ACKNOWLEDGMENTS
 
The support of Bastian Tiemann, Dr med vet, Jörg Graessner, Dipl Phys (Siemens), for optimizing the MR sequences for the animal model, and Volker Schoder, Dipl Stat, for statistical support, is gratefully acknowledged.


   FOOTNOTES
 
See also Science to Practice in this issue.

Abbreviations: CDH = congenital diaphragmatic hernia, FLV = fetal lung volume

Author contributions: Guarantors of integrity of entire study, U.W., H.J.S.; study concepts and design, U.W., M.T., K.H., J.D., G.A., H.J.S.; literature research, U.W.; experimental studies, H.J.S., M.T., U.W.; data acquisition, U.W., M.T., C.H., G.A., H.J.S.; data analysis/interpretation, U.W., M.T., G.A., H.J.S.; statistical analysis, H.J.S.; manuscript preparation, U.W., M.T., C.H., H.J.S.; manuscript definition of intellectual content, K.H., J.D., G.A., H.J.S.; manuscript editing, U.W., H.J.S.; manuscript revision/review, U.W., M.T., C.H., G.A., H.J.S.; manuscript final version approval, U.W., K.H., J.D., G.A., H.J.S.


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 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
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