EXPERIMENTAL STUDY
A new dynamic three-dimensional digital color doppler method for quantification of pulmonary regurgitation: validation study in an animal model
Yoshiki Mori, MD*,
Rosemary A. Rusk, MD*,
Michael Jones, MD ,
Xiang-Ning Li, MD, PhD ,
Timothy Irvine, MD*,
Arthur D. Zetts and
David J. Sahn, MD*,*
* Oregon Health and Science University, Portland, Oregon, USA
The Laboratory of Animal Medicine and Surgery, National Heart, Lung, and Blood Institute, Bethesda, Maryland, USA
Philips Ultrasound, Bothell, Washington, USA
Manuscript received October 17, 2001;
revised manuscript received April 22, 2002,
accepted June 18, 2002.
* Reprint requests and correspondence: Dr. David J. Sahn, The Clinical Care Center for Congenital Heart Disease, Oregon Health and Science University, 3181 SW Sam Jackson Park Road, L608, Portland, Oregon 97201-3098, USA.
sahnd{at}ohsu.edu
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Abstract
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OBJECTIVES: The purpose of the present study was to validate a newly developed three-dimensional (3D) digital color Doppler method for quantifying pulmonary regurgitation (PR), using an animal model of chronic PR.
BACKGROUND: Spectral Doppler methods cannot reliably be used to assess pulmonary regurgitation.
METHODS: In eight sheep with surgically created PR, 27 different hemodynamic states were studied. Pulmonary and aortic electromagnetic (EM) probes and meters were used to provide reference right ventricular (RV) forward and pulmonary regurgitant stroke volumes. A multiplane transesophageal probe was placed directly on the RV and aimed at the RV outflow tract. Electrocardiogram-gated and rotational 3D scans were performed for acquiring dynamic 3D digital velocity data. After 3D digital Doppler data were transferred to a computer workstation, the RV forward and pulmonary regurgitant flow volumes were obtained by a program that computes the velocity vectors over a spherical surface perpendicular to the direction of scanning.
RESULTS: Pulmonary regurgitant volumes and RV forward stroke volumes computed by the 3D method correlated well with those by the EM method (r = 0.95, mean difference = 0.51 ± 1.89 ml/beat for the pulmonary regurgitant volume; and r = 0.91, mean difference = –0.22 ± 3.44 ml/beat for the RV stroke volume). As a result of these measurements, the regurgitant fractions derived by the 3D method agreed well with the reference data (r = 0.94, mean difference = 2.06 ± 6.11%).
CONCLUSIONS: The 3D digital color Doppler technique is a promising method for determining pulmonary regurgitant volumes and regurgitant fractions. It should have an important application in clinical settings.
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Abbreviations and Acronyms
| | ACM | | automated cardiac flow measurement | | ECG | | electrocardiogram | | electrocardiographic | | EM | | electromagnetic | | PA | | pulmonary artery | | PR | | pulmonary regurgitant/regurgitation | | RV | | right ventricle/ventricular | | RVOT | | right ventricular outflow tract | | SGI | | Silicon Graphic Inc. | | 2D | | two-dimensional | | 3D | | three-dimensional | | TOF | | tetralogy of Fallot |
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Deleterious effects of pulmonary regurgitation (PR) on exercise capacity (1,2) and right ventricular (RV) systolic and diastolic function (3–7) have been demonstrated in patients with chronic PR. Some postoperative congenital heart disease patients with chronic PR may need surgical intervention (4,6). Therefore, accurate and noninvasive quantification of PR may be of major clinical importance for the assessment of timing of surgical intervention. Quantitative pulsed Doppler echocardiography has been described for measuring pulmonary regurgitant volumes and regurgitant fractions (8,9). This method, however, is not widely applied for quantifying PR clinically, because of variable results and technical difficulties, especially in determining the precise area of the flow tract (10,11). More importantly, the pulsed Doppler method assumes a flat velocity profile and a constant flow area during the cardiac cycle, but these assumptions are rarely correct. Several studies in normal animals (12,13) and humans (14) have shown that the velocity profiles of forward flow in the main pulmonary artery (PA) are skewed.
Recently, a two-dimensional (2D) computer-assisted semiautomated digital color Doppler method (ACM) has been described, which can avoid having to rely on the assumptions of a flat velocity profile and a constant flow area (15–21). This digital color Doppler method has several advantages for quantifying PR in comparison with the pulsed Doppler method; namely, there is no need for measuring area of the flow tract and using all of the velocity information across the flow diameter to compute instantaneous flow profile. However, the method has a potential limitation because it is generated from a single 2D imaging plane, necessitating an assumption of an axisymmetric circular flow area and uniform velocity profiles in the three-dimensional (3D) space (17–21). Our study using the 2D digital color method indicated that it required data from more than one plane to achieve an accurate result (20,21), presumably because PA flow is complex and flow area is temporally variable. As an extension of this observation, 3D-volume imaging should allow full characterization of complex, dynamic flow velocity profiles.
In this study, we present a newly developed 3D digital color Doppler method that computes the velocity vectors over a segment of a spherical surface perpendicular to the direction of scanning, and we present our evaluation of the 3D digital color Doppler method for determining PR volumes and regurgitant fractions in an animal model with strictly quantified chronic PR.
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Methods
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Animal preparations.
Three to six months before the hemodynamic and ultrasonic study sessions began, we created PR in eight juvenile sheep weighing 18 to 57 kg (mean 43 ± 11 kg). Six of these animals were studied and previously reported in an article about the ACM method (20). Using cardiopulmonary bypass, through a small RV infundibulotomy, the right anterior pulmonary valve cusp was radially incised in one sheep, excised in three sheep, and excised along with left anterior cusp in four sheep, thus producing a wide range of PR severity. All operative and animal management procedures were approved by the Animal Care and Use Committee of the National Heart, Lung, and Blood Institute. Preoperative, intraoperative, and postoperative animal management and husbandry methods are described in detail elsewhere (22).
Electromagnetic flow probe and meters
During the experimental session, the animals underwent median sternotomy under anesthesia with 1% to 2% isoflurane with oxygen. The sheep were intubated and ventilated with a volume-cycle respirator. To obtain PR volume and regurgitant fraction, two electromagnetic (EM) flow probes (model EP455, Carolina Medical Electronics, King, North Carolina) were placed: one around the PA just above the pulmonary valve, and the second around the skeletonized ascending aorta distal to the coronary ostia and proximal to the brachiocephalic trunk. Both flow probes were connected to flow meters (model FM501, Carolina Medical Electronics) and interfaced to the physiologic recorder (Gould ES 2000, Gould Inc., Cleveland, Ohio). All hemodynamic data were recorded at a paper speed of 250 mm/s. Four consecutive cardiac cycles were analyzed for each hemodynamic determination.
To assure reproducibility of the EM flow measurements, the following steps were done: 1) the flow probes and meters were returned to the manufacturer twice a year for in vitro calibration; 2) the similarities of flow were compared when the flow probes on the PA and aorta were switched or the flow meters were switched. In addition, in normal sheep the flows in the PA and aorta were compared, taking into consideration coronary and bronchial arterial flows. Calibration factors for the flow probes were corrected for each animal’s hematocrit levels at each hemodynamic stage, according to the manufacturer’s specifications. The problem of the zero-baseline drift was managed as previously described (23,24). At each hemodynamic stage, the aortic flow zero-level baseline was adjusted according to the contour of its EM flow probe signal; this baseline was reconfirmed by occlusive zero. The aortic zero baseline was stable and did not drift during the course of recording each individual hemodynamic stage. No animal had physiologically important aortic regurgitation or intracardiac shunts. For determination of pulmonary and aortic volumes, the integrals of instantaneous pulmonary and aortic flows over time were determined by planimetry of the flow signal recordings. The baseline value for the pulmonary flow recordings was then adjusted until the forward minus the reversed pulmonary flow volumes equaled the aortic forward flow volumes. The difference between the forward flows represented PR flow volumes. Regurgitant fraction was calculated as diastolic, reversed pulmonary flow volume per minute divided by total forward pulmonary flow volume per minute.
All hemodynamic recordings were performed simultaneously with the echocardiographic studies. One unit (500 ml) of blood was infused in each sheep, producing a 20% average increase in peak aortic flow (an instantaneously observable index of cardiac output). Angiotensin II (Peptide Institute Inc., provided by Tanabe Seiyaku Co., Tokyo, Japan) was infused at a concentration of 20 µg/ml, and nitroprusside at a concentration of 200 µg/ml, at a rate to increase or decrease mean arterial pressure by at least 20%. These interventions were performed to provide a range of hemodynamic states for each animal, not to investigate specific dose-response effects. Thus, a total of 27 stable hemodynamic states were obtained in the eight sheep by altering preload and/or afterload using blood transfusion, sodium nitroprusside, and angiotensin II.
Color Doppler echocardiography and generation of 3D digital velocity datasets
An ATL HDI 5000 (Philips Ultrasound, Bothell, Washington) ultrasound system was used to image the RV outflow tract (RVOT) blood flow running and controlling with a 7 to 4 MHz multiplane transesophageal probe. The probe was placed directly on the RV and aimed at the RVOT, imaging as parallel to the direction of flow as possible. Color gain and filters were adjusted to eliminate random color in areas without flow. Aliasing velocities of 57.7 to 76.9 cm/s were selected to image the RV outflow blood flows. Continuous wave Doppler recordings also were performed to estimate the pressure gradients across the pulmonary annulus.
The HDI 5000 ultrasound system was networked to a Silicon Graphics, Inc. (SGI) workstation via an Ethernet cable connection. Three-dimensional datasets were generated by radial acquisition of 2D cine loops at 6° increments over a 180° rotation of the transducer (30 positions). Images compromising raw scanline data including pre-scan-converted digital velocity information were stored in the HDI 5000 cineloop memory during acquisition. Once the rotation sweep was completed, the digital velocity data from the stored loops acquired at the 30 different angles were transferred to the SGI computer. A custom program, which contained a scan converter, reconstructed the velocity and B-mode volumes separately. The scanning and acquisition of the color Doppler data were gated with the ECG at heart rates ranging from 85 to134 beats/min, but heart rates were relatively constant during each steady stage. Temporal resolution of the 3D reconstructed image (frame rate) was not limited by the 3D method but was between 18 and 24 frames per second with the original color Doppler acquisition frame rates (10 to 15 phases or frames per one cardiac cycle). Image acquisition took about 25 s and data transfer totaled approximately 75 s to accomplish for each stage.
Principle for computation of flow
The principle of our method for computation of flow was as follows. Our method for flow rate computation uses the Gaussian theorem, which states that for any arbitrarily shaped control surface system, the flow rate passing through it equals the summation of all velocity components that are normal to the surface (25). A flow measurement surface (arc-shaped or spherical surface) is chosen such that all points on the surface have equal distance from the transducer. With this, Doppler-measured velocity magnitudes along this surface are precisely the magnitude of the component of the velocity vectors perpendicular to the surface. Sun et al. (15) and Kim et al. (16,26) have previously presented a similar approach, which can measure flow volumes independently of the angle of incidence between the ultrasound beam and the direction of blood flow. The digital velocity information on the 2D spherical surface is acquired at 30 radial positions over a 180° rotation of the transducer, and velocity vectors on the 3D spherical surface are then developed (Fig. 1). Flow rate through the entire surface can be estimated by simply summing the incremental surface areas multiplied by their respective Doppler measured velocities. Thus, computation of the instantaneous flow rate was generated by integrating the velocity vectors over a selected 3D spherical surface at each phase.
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Figure 1 Examples of selected three-dimensional velocity vectors of the forward flow in the right ventricular outflow tract (top) and the pulmonary regurgitation (PR) flow in the pulmonary artery (bottom). Note that the magnitudes of the components of the velocity vectors of the forward flow and PR flow were not the same.
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Data analysis
Display and computation of the datasets were performed off line using a dedicated software program on a UNIX SGIO2 computer. The program displayed a dynamic mode of the color Doppler image and B-mode image on the sample surface onto a projection—a view that is similar to the cross-sectional cut that facilitates spatial and temporal segmentation of the flow field and flow phase (Fig. 2). The flow rate and stroke volume was calculated interactively. The program could extract velocities from digital 3D datasets and display velocity vectors as 3D objects in flat or curved planes as described above (Fig. 1). Using the software program, the user could define the position of the arc on the dynamic mode of the color Doppler image, from which the 3D spherical surface would be developed, and then the flow area of interest could be defined. The flow rate curve through the cardiac cycle was derived by automatically demarcating the flow area and velocities and then integrating them through systolic and diastolic phases over one cardiac cycle. The program allows manual corrections to the automatically detected flow area. To obtain the regurgitant flow volumes, the sampling arc corresponding to the 3D spherical surface was placed distal to the pulmonary valve (Fig. 2). A total of five to seven phases during diastole were selected, and cross-sectional areas of the PA then were corrected manually so as to obtain the actual flow rates excluding color noise. The regurgitant volumes were computed to integrate the instantaneous flow rates over time during diastole. To obtain the RV forward flow volumes, the sampling arc was placed just proximal to the pulmonary valve (Fig. 2). In a similar fashion, a total of five to eight phases during systole were selected. The RV forward stroke volumes then were obtained by measuring the cross-sectional areas and digital color Doppler signals of the RVOT and integrating the flow rates at each phase during systole. The total time of off-line measurements for each regurgitant volume or RV forward stroke volume was within 3 min. The PR fraction was calculated as the ratio of the regurgitant volume per beat to the RV forward volume per beat.
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Figure 2 Examples of selected images of the pulmonary regurgitation (PR) flow (upper panel) and right ventricular forward flow (bottom panel). The program displayed the dynamic B-mode of the color Doppler image (left panel) and the cross-sectional area on the sample surface (right panel). The sampling arc was placed distal to the pulmonary valve for measurements of the PR flow volumes (upper left), and the flow rate curve at this point over one cardiac cycle was displayed (bottom in the upper panel). The sampling arc was placed proximal to the pulmonary valve for measurement of the right ventricular forward flow volumes (bottom left). Note that color-encoded velocity distribution in the cross-section of the right ventricular outflow tract (RVOT) and pulmonary artery (PA) is not uniform (dark and light). This indicates that the velocity profiles of both forward flow in the RVOT and PR flow in the PA are not uniform in the three-dimensional space.
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Interobserver variability
To evaluate the effect of interobserver variability on measurement of regurgitant volume and RV forward volume, two investigators independently performed measurements on 10 randomly selected flow conditions. The two independent investigators were blinded to the knowledge of images selected, the results obtained by the other observer or reference EM data.
Statistical analysis
All values are expressed as mean values ± SD. Simple linear regression analysis was used for obtaining correlation coefficients between the values derived by the 3D method and reference data. Agreement with two measurements was tested according to the Bland-Altman method (27). The data obtained by the 3D method were also compared with the reference data using paired Student t test. A p value <0.05 was considered statistically significant.
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Results
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Severity of pulmonary stenosis and regurgitation.
One sheep had mild but significant pulmonary stenosis in which the peak pressure gradients across the pulmonary annulus calculated by applying the simplified Bernoulli equation ranged from 16 to 36 mm Hg (average 31 ± 6 mm Hg). For the other sheep, peak velocities across the pulmonary annulus determined by continuous-wave Doppler ranged from 0.6 to 1.8 m/s (average 1.1 ± 0.3 m/s), documenting minimal narrowing at the annulus. All PR jets were eccentric. Pulmonary regurgitation fractions obtained by the EM method were within clinically relevant ranges from 9.8% to 75% (average 37 ± 18%).
Estimation of regurgitant volumes and regurgitant fractions
Simple regression analysis showed that the regurgitant volumes derived by the 3D method correlated and agreed well with those obtained by the EM method (r = 0.95, SEE = 1.89 ml/beat, p < 0.0001, mean difference = 0.51 ± 1.89 ml/beat) (Fig. 3). Good correlation and agreement between the RV stroke volumes determined by the 3D method and those by the EM method were also demonstrated (r = 0.91, SEE = 3.36 ml/beat, p < 0.0001, mean difference = –0.22 ± 3.44 ml/beat). There was no significant difference in the PR volumes and the RV stroke volumes between the 3D method and the EM method (p = 0.17 for the regurgitant volumes, p = 0.75 for the RV stroke volumes). As a result of these measurements, the PR fractions correlated and agreed well with those by the EM method (r = 0.94, SEE = 5.90%, p < 0.0001). The range of agreement for the difference between the regurgitant fraction by the 3D method and that by the EM method was 2.06 ± 12.22% (mean ± 2 SD). There was also no significant difference between the 3D-derived regurgitant fractions and the reference data (p = 0.09) (Fig. 4).
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Figure 3 (A) Simple linear regression analysis of regurgitant volumes obtained by the electromagnetic (EM) flow meters versus those by the three-dimensional (3D) digital color Doppler method. (B) Agreements of regurgitant volumes obtained by the EM flow meters versus those by the 3D digital color Doppler technique according to the Bland-Altman method.
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Figure 4 (A) Simple linear regression analyses of regurgitant fraction obtained by the electromagnetic (EM) flow meters versus those by the three-dimensional (3D) digital color Doppler method. (B) Agreements of regurgitant fractions obtained by the EM flow meters versus those by the 3D digital color Doppler technique according to the Bland-Altman method.
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Interobserver variability
One observer obtained 11 ± 3 ml/beat of regurgitant volume and 32 ± 6 ml/beat of RV stroke volume. Another observer obtained 13 ± 3 ml/beat of regurgitant volume and 29 ± 6 ml/beat of RV stroke volume. Thus, there was good agreement between the two independent observers’ measurements of regurgitant volumes (r = 0.88, p < 0.0001, SEE = 1.6 ml/beat, mean absolute difference = 1.49 ± 1.53 ml/beat), and RV stroke volumes (r = 0.93, p < 0.0001, SEE = 2.5 ml/beat, mean absolute difference = 2.64 ± 2.43 ml/beat).
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Discussion
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Deleterious effects of chronic PR on exercise performance and RV function are now accumulating (1–3,5,7). Carvalho et al. (2) demonstrated that impaired exercise capacity after repair of tetralogy of Fallot (TOF) was directly related to the degree of chronic PR and that patients with PR fraction of about 40% showed abnormal maximal oxygen uptake as an indicator of exercise ability. Recently, Rahman et al. (7) studied patients with TOF after surgical repair and showed that patients with severe PR had a lower RV ejection fraction and impaired combined systolic-diastolic global function than patients with mild-to-moderate PR. In an effort to halt the progression of RV volume load, several centers have restored pulmonary valve competence (4,6). Ilbawi et al. (4) reported that patients who had undergone a repair of TOF, and who had moderate PR (32%, PR fraction), recovered RV function after the insertion of a pulmonary valve. Although clear criteria of surgical intervention for chronic PR have not been shown yet, postoperative follow-up of TOF or other disease clearly requires a non-invasive technique that is suitable for repetitive study. The ultrasound method that can accurately quantify PR could be suitable to answer this clinical request.
Our new 3D digital color Doppler method.
In the present study, we used a technique conceptually similar to the magnetic resonance velocity mapping method (28) described previously, which measures regurgitant flow directly. Our dynamic 3D digital color Doppler method derives the instantaneous flow rate by integrating the product of the flow area and its associated raw digital Doppler velocities projected on a segment of a spherical flow surface. The spherical surface is perpendicular to both the directions of the flow and the flow interrogation. Although we imaged parallel to the direction of flow, a misalignment of the Doppler beam orientation with flow direction may occur because of difference in the angle between forward and regurgitant flow direction in the PA. However, this spherical approach is less dependent on the angle of the incidence between the ultrasound beam and the direction of blood flow, as shown by Sun et al. (14) and Kim et al. (15,25). Our previously performed in vitro study with this 3D method showed that it estimated flow rates and stroke volumes accurately compared with the reference data obtained by an ultrasonic flow meter, when the angle between the ultrasound beam and the direction of flow was  50° (29). Our 3D method also accounts for the dynamically changing vessel area and uses all of the velocity information through the flow area to compute instantaneous flow profiles. More importantly, the 3D method does not make any assumptions about geometry or flow profiles. Furthermore, the velocity profile across the prestenotic region is not flat in the presence of pulmonary valvar stenosis (19), and as a result of variable orifice position and PA curvature, the spatial velocity distribution of the regurgitant flow is not uniform. In fact, the velocity profiles of both forward flows in the RVOT and regurgitant flow in the PA were not flat, as shown in Figures 1 and 2. Our study demonstrated that the dynamic 3D digital color Doppler method provided accurate RV forward stroke volumes, PR volumes, and regurgitant fractions even when the cross-sectional flow area was not axisymmetric and the flow profiles were complex. We also have data from another study of the 3D digital Doppler method that show that the PR volumes obtained by the indirect subtraction method (PR volumes calculated by subtracting the systemic from the RV stroke volumes) agreed well with the reference data (30). Thus, our 3D digital color Doppler allows full characterization of complex, dynamic flow velocity profiles in various cardiac locations.
Comparison of 3D versus 2D digital color Doppler method for quantifying PR
Our previous study showed that the 2D digital color Doppler method that used the average of two orthogonal planes could estimate more accurately the actual RV stroke volumes and PR volumes than it did by using a single plane (20). However, the method using the average of two orthogonal planes slightly but significantly overestimated the RV stroke volumes and PR volumes in the same animal model as described in our previous study of the ACM method (RV stroke volume: mean difference = +2.97 ± 2.69 ml/beat and mean degree of overestimation = 111 ± 10%; PR volume: mean difference = +1.79 ± 1.84 ml/beat and mean degree of overestimation = 134 ± 57%) (20). In contrast, the dynamic 3D digital color Doppler method did not overestimate or underestimate the reference data but provided the actual RV forward stroke volumes and PR volumes, and as a result, it provided accurate regurgitant fractions. In addition, in our in vitro physiologic porcine PA model, eight different pulsatile flow volumes (20 to 55 ml/beat) measured by ultrasonic flow meter were examined, and we compared the 2D versus the 3D digital color Doppler method to determine which more accurately estimated flow volumes in an asymmetrical geometry tract such as the PA. We have data from this study that demonstrate that the flow volumes in main PA by the 2D method using averages of two orthogonal planes showed wide variability compared with our 3D method (r = 0.92, SEE = 5.8 ml/beat, mean difference = 1 ± 6 ml/beat for the 2D vs. r = 0.98, SEE = 2.1 ml/beat, mean difference = 0.2 ± 2 ml/beat for the 3D, unpublished data). Thus, our 3D approach could provide a more accurate quantification of PR than the 2D method, even when the average of two orthogonal planes is used.
Regarding the relationship between the number of 3D planes and resultant accuracy of the assessment of regurgitant fraction, it is probably different for the aorta versus the PA. For the aorta, which has more symmetry of flow, 18 samples over 180° appears sufficient, and for the pulmonary artery, at least 30 samples over 180° is the minimum sampling density we have found that yields reproducible data beat to beat.
Limitations
Some limitations in the present study should be considered. First, we performed epicardial echocardiography to obtain high-quality images, because the digital color Doppler method depends on the quality of color flow mapping. In the clinical setting, it can be difficult to obtain such high-quality images; however, previously performed intraoperative transesophageal studies with the 2D digital color Doppler method have shown that the RVOT flows can be imaged in patients with similar quality (31,32). Second, the potential influence of various instrument settings was not investigated in our 3D digital color Doppler method. In vitro and clinical studies with the 2D digital color Doppler have shown the effect of color gain settings, wall filters, frame rates, pulse repetition frequency, and depth of the region of interest (17,18). We sampled at the different depth for measuring the forward and regurgitant flow volumes, because the digital color Doppler method requires nonaliasing and laminar flow signals. As a result, the variation in the lateral resolution at the different depth may be a source of the error, although the depth of sampling position for the forward and regurgitant flows was close. However, our previous studies with 2D digital color Doppler method using the same technique have shown that the forward and the regurgitant flow volumes can be measured with a high level of accuracy (18,20). Thus, the problem of the lateral resolution can be minimal. Further study will be required to clarify the influence of those instrument effects.
Finally, our 3D method used ECG-gated acquisition but did not provide for respiratory gating. Also, the 3D method at present requires off-line processing. This type of computation, however, should eventually be applied to real-time 3D echo with color flow mapping, which should allow the flow calculation to be made directly on a beat-to-beat basis, as long as the sampling rate is high and the velocity assessment accurate.
Conclusions
Our 3D digital color method can accurately quantify RV forward stroke volumes, PR volumes, and regurgitant fractions. This should be of clinical importance in patients with congenital heart disease such as postoperatively repaired TOF, as well as in patients with valvular heart disease or pulmonary hypertension.
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Acknowledgments
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We acknowledge the assistance of veterinary professional and technical staff of the Laboratory of Animal Medicine and Surgery, National Heart, Lung, and Blood Institute. We would also like to thank Judy Schultheis for her assistance with the preparation of the manuscript.
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