Fetal lung volume determination by three-dimensional ultrasonography Andreas Lee, MD, Alfred Kratochwil, MD, Ingrid Stimpflen, Josef Deutinger, MD, and Gerhard Bernaschek, MD Vienna, Austria OBJECTIVE: Pulmonary hypoplasia is common in compromised pregnancies. However, prenatal diagnosis by volume measurement has not become routine until now. The performance of three-dimensional ultrasonography in fetal lung volume determination was evaluated in this study. STUDY DESIGN: In a total of 78 singleton pregnancies 108 measurements were performed. Lung volume was calculated by subtraction of the fetal heart volume from the volume of the fetal thorax. RESULTS: Linear regression of transformed fetal lung volume growth gave best results (R 2 = 0.77, p < 0.001), ranging from 2.8 ml at 14 weeks' gestation to 148 ml at term. CONCLUSION: Three-dimensional ultrasonography provides not only access to surface rendered images but it also enables more sophisticated volume measurements. In this study three-dimensional ultrasonography provided fast, easy access for volume estimation of the fetal lung. This technique can be used to reasonably predict fetal lung volume. (Am J Obstet Gynecol 1996;175:588-92.) Key words: Three-dimensional ultrasonography, fetal lung volume, biometry, fetal growth Accurate measurement of fetal organ volumes has not been routine until now. The prenatal determination of volume parameters would be useful in assessing fetal growth and maturity, especially in cases of fetal malforma- tion. Measurement of fetal lung volume would offer new possibilities in managing pregnancies compromised be- cause of malformations (e.g., fetal lung hypoplasia) or in cases of preterm delivery, where fetal lung maturity plays an important role. Only a few reliable data of fetal lung volume are given by postmortem studies.' 2 Volume mea- surement by two-dimensional ultrasonography is limited to inaccurate and approximating methods (e.g., biplane Simpson mode). 3 Ellipse integration volume measure- ment is primarily used for measurement. In this method an ellipse that approaches the real extension of the object is calculated. Still, this ellipse does not match the real volume. In a recent study fetal lung volume has been measured by echo-planar magnetic resonance imaging (MRI), showing an exponential increase of lung volume ranging from 21 ml at 23 weeks' gestation to 94 ml at term. 4 ' 5 However, examinations of the fetus in utero by MRI is limited because of relatively long acquisition times, artifacts caused by fetal movements, high cost, and From the Department of Prenatal Diagnosis and Therapy, University of Vienna. Received for publication October 9, 1995; revised January 29, 1996; accepted January 30, 1996. Reprint requests: Andreas Lee, MD, AKH University Hospital Vienna, Department of Prenatal Diagnosis and Therapy, Waehringer Guertel 18-20, 1090 Vienna, Austria. Copyright by Mosby-Year Book, Inc. 0002-9378/96 $5.00+ 0 6/1/72478 limited acceptance of pregnant women. Three-dimen- sional ultrasonography for imaging of the fetus is now available, and this technique offers easy, fast access to any possible view and accurate determination of fetal organ volume and surface and volume rendering."' In contrast to two-dimensional ultrasonography, three-dimensional ultrasonography allows determination of organ volume by stepping through organs slice by slice. In each plane of the object the area was traced by means of a cursor. Calculation of the total volume was then performed by building the sum of each slice's volume. Accuracy of three-dimensional volume determination has been stud- ied and measurement error has been reported ranging from +8% to -6.1%."' 2 Our study describes the applica- tion of three-dimensional ultrasonography to obtain fetal lung volume. Patients and methods A total of 108 measurements in 78 pregnant women admitted to our department for ultrasonographic screen- ing were performed in this study. All the women gave informed permission for three-dimensional ultrasono- graphic examination. None had diabetes or any other systemic disease. Singletons without fetal malformations and with normal fetal growth were included. Gestational age had been verified by first-trimester ultrasonography. The mean gestational age was 27 weeks (range 14 to 41 weeks). Measurements of the fetus were repeated after a mean interval of 36 days (range 7 to 85 days). The technical equipment consisted of a Combison 530 ultrasonography machine (Kretztechnik, Zipf, Austria) 588
Andreas Lee, MD, Alfred Kratochwil, MD, Ingrid Stimpflen, Josef Deutinger, MD, andGerhard Bernaschek, MD
Vienna, Austria
OBJECTIVE: Pulmonary hypoplasia is common in compromised pregnancies. However, prenataldiagnosis by volume measurement has not become routine until now. The performance ofthree-dimensional ultrasonography in fetal lung volume determination was evaluated in this study.STUDY DESIGN: In a total of 78 singleton pregnancies 108 measurements were performed. Lungvolume was calculated by subtraction of the fetal heart volume from the volume of the fetal thorax.RESULTS: Linear regression of transformed fetal lung volume growth gave best results (R2 = 0.77,p < 0.001), ranging from 2.8 ml at 14 weeks' gestation to 148 ml at term.CONCLUSION: Three-dimensional ultrasonography provides not only access to surface rendered imagesbut it also enables more sophisticated volume measurements. In this study three-dimensionalultrasonography provided fast, easy access for volume estimation of the fetal lung. This technique can beused to reasonably predict fetal lung volume. (Am J Obstet Gynecol 1996;175:588-92.)
Accurate measurement of fetal organ volumes has notbeen routine until now. The prenatal determination ofvolume parameters would be useful in assessing fetalgrowth and maturity, especially in cases of fetal malforma-tion. Measurement of fetal lung volume would offer newpossibilities in managing pregnancies compromised be-cause of malformations (e.g., fetal lung hypoplasia) or incases of preterm delivery, where fetal lung maturity playsan important role. Only a few reliable data of fetal lungvolume are given by postmortem studies.' 2 Volume mea-surement by two-dimensional ultrasonography is limitedto inaccurate and approximating methods (e.g., biplaneSimpson mode).3 Ellipse integration volume measure-ment is primarily used for measurement. In this methodan ellipse that approaches the real extension of the objectis calculated. Still, this ellipse does not match the realvolume. In a recent study fetal lung volume has beenmeasured by echo-planar magnetic resonance imaging(MRI), showing an exponential increase of lung volumeranging from 21 ml at 23 weeks' gestation to 94 ml atterm.4' 5 However, examinations of the fetus in utero byMRI is limited because of relatively long acquisitiontimes, artifacts caused by fetal movements, high cost, and
From the Department of Prenatal Diagnosis and Therapy, University ofVienna.Received for publication October 9, 1995; revised January 29, 1996;accepted January 30, 1996.Reprint requests: Andreas Lee, MD, AKH University Hospital Vienna,Department of Prenatal Diagnosis and Therapy, Waehringer Guertel18-20, 1090 Vienna, Austria.Copyright by Mosby-Year Book, Inc.0002-9378/96 $5.00+ 0 6/1/72478
limited acceptance of pregnant women. Three-dimen-sional ultrasonography for imaging of the fetus is nowavailable, and this technique offers easy, fast access to anypossible view and accurate determination of fetal organvolume and surface and volume rendering."' In contrastto two-dimensional ultrasonography, three-dimensionalultrasonography allows determination of organ volumeby stepping through organs slice by slice. In each plane ofthe object the area was traced by means of a cursor.Calculation of the total volume was then performed bybuilding the sum of each slice's volume. Accuracy ofthree-dimensional volume determination has been stud-ied and measurement error has been reported rangingfrom +8% to -6.1%."' 2 Our study describes the applica-tion of three-dimensional ultrasonography to obtain fetallung volume.
Patients and methods
A total of 108 measurements in 78 pregnant womenadmitted to our department for ultrasonographic screen-ing were performed in this study. All the women gaveinformed permission for three-dimensional ultrasono-graphic examination. None had diabetes or any othersystemic disease. Singletons without fetal malformationsand with normal fetal growth were included. Gestationalage had been verified by first-trimester ultrasonography.The mean gestational age was 27 weeks (range 14 to 41weeks). Measurements of the fetus were repeated after amean interval of 36 days (range 7 to 85 days).
The technical equipment consisted of a Combison 530ultrasonography machine (Kretztechnik, Zipf, Austria)
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Lee et al. 589Volume 175, Number 3, Part 1AmJ Obstet Gynecol
Fig. 1. Imaging of fetus in three simultaneous perpendiculous planes. Upper left corner Transversesection; upper right corner sagittal section; lower left corner, frontal section. Area tracing of fetal thorax incross-section plane. Vertebrae and ribs are excluded. Cross-sectional planes of fetal thorax are visualizedas several consecutive slices after three-dimensional ultrasonographic volume sampling.
Fig. 2. Fetal heart volume determination after three-dimensional volume sampling.
590 Lee et al. September 1996AmJ Obstet Gynecol
Fig. 3. Growth chart of total fetal lung volume versus gestational age. Regression line with 95% confi-dence intervals is drawn.
with a built-in graphic processor and software 3D-View(Kretztechnik). We used a 5 MHz annular array trans-ducer with an integrated electromechanical device forvolume scanning. The pyramidal volume box was limitedto a maximum of 20 cm long x 9 cm wide x 13 cm deep
(2500 cm3). The opening angle of each plane was 90degrees and the angle of volume sampling was limited toa maximum of 60 degrees. Within this volume box a
maximum resolution of 250 slices per volume box couldbe obtained, each slice consisting of 160 x 160 voxels.Sampling of one volume box took an average of 2 sec-onds. All volume data were stored and processed by theultrasonography machine. The volume could be evalu-ated slice by slice in any arbitrary plane. The three-di-mensional view software allowed volume display on themonitor in three simultaneously perpendicular planes.Volume measuring was performed by area tracing incross-section planes of the fetal thorax. For standardizingmeasurements in this study the limits of the fetal thoraxhad been determined between clavicle and diaphragm.Lung volume was calculated by measuring fetal thorax intwo steps. The first parameter obtained was the volume ofthe thorax excluding vertebrae and ribs (Fig. 1). Then, asa second parameter, fetal heart volume was determinedby use of the fetal heart circumference in each cross-section of fetal thorax (Fig. 2). Both volumes were calcu-lated with the integrated three-dimensional software vol-ume measuring method. Each measurement was re-peated and the mean values were taken as the result.
Finally, the total fetal lung volume was calculated by sub-traction of fetal heart volume from the first parameter. Allmeasurements were performed by one physician to elimi-nate variations in examiner technique. At the time ofexamination results of previous fetal lung volume mea-surements were not available to disallow arbitrary correc-tions of volume calculations. All data of fetal lung vol-umes were plotted against gestational age. To allow con-trol of the calculated trend line against individual fetalgrowth curve, each set of patient data was drawn in thechart. Regression analysis was applied after square roottransformation to stabilize variance. The resulting equa-tion for regression line was used to calculate the meanand residual SD in transformed units. Reference rangeswere produced by power transformation. Statistical anal-ysis was performed by software SPSS, version 5.0.2 (SPSSInc., Munich).
Results
Fetal lung volume. obtained by three-dimensional ul-trasonography ranged from 2.4 ml (14 weeks' gestation)to 148 ml (at term) (Fig. 3, Table I). Calculation of thelinear regression line (lung volume vs gestational age)gave y = a + b weeks ( = 0.77) (Table II). Student t testcalculation revealed p < 0.001. In only two cases the indi-vidual growth curve is crossing the trend line, showing anunusual change in fetal growth (Fig. 4).
Fetal lung volume calculation took an average of 15minutes for each patient, starting from volume sampling
until the end of calculation (a total of four single mea-surements). Deviation between each repeated measure-ment ranged from 0.1 to 15 ml, whereas differences be-
tween measurements were small in early pregnancy andincreased until the end of pregnancy.
Comment
Until now only a few data on fetal lung volume growthare available. MRI studies are expensive and fetal move-ment can cause severe artifacts during imaging. Measure-ments of fetal organs by two-dimensional ultrasonogra-phy can be inaccurate because of the need of averaging
algorithms. Three-dimensional ultrasonography cansolve this problem by determining volumes by a newtechnique, which is already known by other three-dimen-sional imaging procedures. In our study we examinedfetal lung growth by volume measurements. This tech-nique still has several limitations that have to be consid-ered. Accuracy of three-dimensional volume measure-ments is satisfying as long as good resolution can be
obtained. In cases of low imaging quality (e.g., because ofobesity) fetal lung volume determination could not beperformed. Analogous to two-dimensional ultrasonogra-phy bones could cause shadows on some parts of fetalstructures. As long as these artifacts were limited to fewslices inside the volume box, they did not influence theresult markedly. Accuracy in three dimensional volumemeasurements also may depend on position of the fetusand the distance from the fetus to the transducer. Reso-lution increased with an increase of the sampling rate and
Table I. Range for fetal lung volume measuredby three-dimensional ultrasonography
cannot be excluded. Although scanning of the fetal tho-rax was performed, fetal heart movements were frozen.During measurement and stepping through the fetal tho-rax slice by slice different stages of heart contractioncould be found. Therefore measurement of the fetal heart
was done partly during diastole and partly during systole.The resulting fetal heart volume represented a meanvalue between maximum and minimum heart volume.
The extent of the fetal lung has been limited to anupper plane, which is located at fetal clavicles, and alower plane, located at the fetal heart apex. This was
somewhat arbitrary, but it gave the best reproduciblelandmarks for measurements. Especially when the fetalthorax reached the maximum size of the available volume
box, orientation by these landmarks was useful.Fetal lung volume was calculated by subtraction of fetal
heart volume from fetal thorax volume, which includedlungs, vessels, and heart but excluded vertebrae and ribs.Therefore both lungs, parts of vessels, and parts of thethymus gland represented the result of calculation.
To exclude a possible effect on the results resultingfrom information about clinical data, we made specialefforts to exclude this source of inaccuracy.
Individual lung growth of patients compared with theregression line helps prove the resulting growth chart. Ina few patients, either because of rapid changes of lunggrowth or because of error in measurement, the valuescrossed the regression line.
Although three-dimensional ultrasonography mostly isassociated with surface rendering images, in clinical rou-tine it may be useful for volume measurements. Themethod of examination of the patient has not changed inregard to two-dimensional ultrasonograpy, and volumesampling is performed in only few seconds. Thereforefetal exposure to ultrasonography can be reduced. Dur-ing examination the ultrasonography power output wasexactly the same as in two-dimensional ultrasonography.All data could be stored and volume measurement couldbe repeated any time.
Fetal lung volume can be useful in determining lungmaturity, especially in cases of malformation (e.g., dia-phragmatic hernia, lung hypoplasia, congenital adenoi-dal malformations, and hydrothorax). In such cases man-agement of fetal therapy or timing of delivery may beimproved. Further studies are necessary. Our experiencewith this technique seems to be promising. Three-dimen-sional ultrasonography may be useful in fetal organ vol-ume determination in the near future.
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