The left and right atria have numerous functions; therefore, accurate measurement of atrial size is critical in the assessment of patients for the presence and extent of heart disease. An increase in atrial size generally refects changes in pressure or volume in a physiologic attempt to compensate for an increase in atrial wall stress. The extent of atrial dilation is often predictive of adverse cardiovascular outcomes; thus, the importance of accurate quantification of atrial size cannot be understated.
Atrial size can be noninvasively assessed by use of echocardiography. Echocardiography is fairly widely available in veterinary practice and provides veterinarians the ability to subjectively and objectively assess atrial size. Objective measurements include linear dimensions and area and volume calculations. Unfortunately, a single linear measurement is an insensitive method for quantification of atrial size owing to the complex geometry of both atrial chambers and the potential for eccentric enlargement of the atria.1 Atrial volume is superior to linear measurements for quantification of atrial size. One- and 2-D echocardiographic techniques can be used to estimate atrial volume by means of mathematical formulas and geometric shape assumptions, whereas 3DE directly measures atrial volume.
The left and right atria have different shapes with appendages and venous connections that should be distinctly considered. Objective echocardiographic quantification of left atrial size has been the focus of multiple studies.2–4 In those studies,2–4 the limitations associated with the use of a single linear dimension for estimation of left atrial size were underscored and clinical assessment of LAV was advocated. The left atrium is a complex structure that can enlarge eccentrically in multiple planes. In veterinary studies,2–4 left atrial size was evaluated with various echocardiographic techniques, but echocardiographic measurements were not compared with a volumetric gold standard. Thus, in veterinary medicine, the relationship between the LAV determined by echocardiographic methods and the LAV determined by a volumetric gold standard has not been established. In humans, LAV determined by 3DE closely agrees with that determined by cMRI and MDCT.5,6 Generally, the LAV derived from 3DE is more closely correlated with that determined by cMRI than the LAV derived from 2DE, although in humans, the LAV is systematically underestimated by both echocardiographic modalities.7,8
The veterinary literature contains little information regarding quantitative assessment of right atrial size. In 1 study,9 the right atrial size of dogs was measured by use of area and length measurements obtained by 2DE. Studies are lacking regarding measurement of RAV in dogs. In human medicine, right atrial size is most accurately assessed with advanced cross-sectional imaging techniques, with cMRI considered the gold standard for quantification of right atrial size.10 Results of multiple human studies11,12 indicate that the RAV determined by cross-sectional imaging techniques is greater than that determined by echocardiography. Current ASE guidelines13 recommend that the right atrial area be measured from the LAP window because of the paucity of standardized RAV data derived by 2DE. That recommendation may soon change because reference ranges for RAV have been subsequently established by use of 2DE and 3DE methods.14,15
To our knowledge, LAVs and RAVs quantified by 2DE and 3DE have not been compared with those determined by a volumetric gold standard for veterinary species. The aim of the study reported here was to compare the LAVs and RAVs derived from 2DE and 3DE with those derived from MDCT for healthy dogs. We hypothesized that the LAV and RAV measured by both 2DE and 3DE would underestimate the corresponding volumes measured by MDCT (gold standard). We also hypothesized that, although the MDCT-derived volume would be similar between left and right atria, the magnitude by which 2DE underestimated RAV would be greater than that for LAV owing to limitations associated with obtaining adequate images for accurate measurement of the right atrium by 2DE.
Materials and Methods
Animals
Eleven sexually intact (7 males and 4 females) young adult purpose-bred hound-type dogs with a mean ± SD body weight of 19.9 ± 2.6 kg were evaluated in the study. Dogs were owned by either Oregon State University or a private entity that provided consent for the dogs to be enrolled in the study. All study procedures were reviewed and approved by the Oregon State University Institutional Animal Care and Use Committee. Dogs were considered healthy on the basis of results of a physical examination, CBC, serum biochemical analysis, and ECG and complete echocardiographic evaluations.
Anesthesia
Dogs were anesthetized during both ECG-gated MDCT and echocardiographic imaging. For the first 5 dogs evaluated, the sequence in which the imaging modalities were performed was randomized by pulling numbers from a hat. For the remaining 6 dogs, MDCT was performed before echocardiography. Each dog was sedated with butorphanol tartrate (0.1 to 0.2 mg/kg, IM), and a catheter was aseptically placed in a cephalic vein. Anesthesia was induced with propofol (3 to 5 mg/kg, IV, titrated to effect). Following endotracheal intubation, anesthesia was maintained with isoflurane delivered in oxygen. Lactated Ringer solution (10 mL/kg/h, IV) was administered for the duration of anesthesia.
ECG-gated MDCT
Dogs were positioned in sternal recumbency, and ECG electrodes were attached to the forelimbs and left hind limb in a routine manner. Contrast-enhanced MDCT images were acquired by use of a 64-row detector CT scannera and the following settings: collimation, 0.5 mm; reconstruction interval, 0.5 mm; matrix, 512 × 512; field-of-view display, 163 to 213 mm; pitch factor, 0.829; gantry rotation speed, 350 milliseconds; tube voltage, 120 kV; tube current, 200 to 500 mA; and tilt angle, 0°. Images were acquired following administration of iopamidolb contrast medium by use of a dual-barrel power injector.c A 3-phase injection protocol was used for the first 5 dogs evaluated. That protocol consisted of an initial fast flow rate (5 mL/s) of contrast medium, a second slower flow rate (2 mL/s) of contrast medium, and a final fast flow rate (5 mL/s) of sterile saline (0.9% NaCl) solution. Each of those 5 dogs had 2 separate contrast medium injections. For each injection, the total dose of contrast agent administered was 1 mL/kg, and the total dose of saline solution administered was 0.5 mL/kg. For contrast-enhanced visualization of the left side of the heart, automated bolus tracking initiated scanning when a radiodensity of 180 HU was detected in the ascending aorta. For contrast-enhanced visualization of the right side of the heart, automated bolus tracking initiated scanning when a radiodensity of 130 to 160 HU was detected in the main pulmonary artery. For the last 6 dogs evaluated, a modified contrast medium injection protocol was used, which allowed for opacification of all 4 chambers of the heart with a single injection. That protocol consisted of an initial fast flow rate (3 mL/s) of contrast medium, a second slower flow rate (2 mL/s) of contrast medium, and a final injection of sterile saline solution (2 mL/s). For each of those 6 dogs, the total dose of contrast medium administered was 1.5 mL/kg and total dose of saline solution administered was 1.0 mL/kg. Automated bolus tracking initiated scanning when a radiodensity of 140 HU was detected in the ascending aorta. Immediately prior to each scan, a breath hold was achieved by delivering peak end inspiratory pressure and temporarily suspending mechanical ventilation during MDCT image acquisition.
The MDCT images were transferred to a server for offline analysis at a workstation with softwared for calculation of LAV and RAV. Images were reconstructed at 10% increments of the R-R interval. Multiplanar reconstructed images were created to display long- and short-axis views of the left and right atria. The functional analysis software displayed the 4-chamber, 2-chamber, and short-axis views of the atria with automated regions of interest for contrast detection. On the long-axis and short-axis images of the left (Figure 1) and right (Figure 2) atria, the region of interest was manually adjusted to include the entire atrium. All manual adjustments were made by 1 investigator (NLL). Following manual adjustment of the regions of interest, the software computed the LAV and RAV for each 10% increment of the R-R interval. The software generated 1 cardiac cycle from the CT scan; therefore, the MDCT-derived LAV and RAV for each dog were calculated once by 1 observer (NLL). For each atrium, volume was defined as the maximal volume for the entire cardiac cycle. For each dog, both the LAV and RAV were recorded as the raw volume (mL) and volume indexed to body weight (mL/kg). Additional scans that would have yielded multiple measurements for each dog were not obtained to minimize radiation exposure and avoid potential deleterious consequences associated with repeated injection of the iodinated contrast medium (eg, contrast-induced nephropathy).
Echocardiography
Each dog underwent a comprehensive echocardiographic examination that included M-mode, 2-D, pulsed-wave Doppler, and 3-D imaging with continuous ECG monitoring. All examinations were performed by 1 board-certified veterinary cardiologist (NLL) who used a single ultrasound unit.e For each 2-D imaging plane, a 5-beat loop was recorded while optimizing the field of view to image each atrium. Volumetric measurements of each atria were performed for 3 consecutive beats.
Left atrial volume was measured in triplicate by 2DE. It was measured on long-axis 4-chamber views obtained through the RPS and LAP windows at ventricular end systole in the last frame obtained before mitral valve opening in accordance with ASE recommendations.1 On both the RPS and LAP views, the endocardial border of the left atrium was manually outlined with care taken to exclude the pulmonary veins and left atrial appendage. The ventral border of the left atrium was identified by observation of the hinge points of the mitral valve. Single-plane volume estimates were obtained from the RPS and LAP views by use of the MOD.
Right atrial volume was also measured in triplicate by 2DE. It was measured on LAP and LCR views at ventricular end systole in the last frame obtained before tricuspid valve opening. The LAP and LCR views were optimized for measurement of the right atrium. The LAP views were obtained as described9 with slight cranial angulation and counterclockwise rotation of the probe at a more cranioventral location on the left thoracic wall. On both the LAP and LCR views, the endocardial border of the right atrium was manually outlined with care taken to exclude the cavae and right atrial appendage. The ventral border of the right atrium was identified by observation of the hinge points of the tricuspid valve. Single-plane volume estimates were obtained from the LAP and LCR views by use of the MOD.
All 3DE data were obtained with a 1-MHz or 5-MHz matrix transducer. Echocardiographic images were acquired in wide-angled full-volume acquisition mode from the LAP window and were optimized for each atrium over 4 consecutive cardiac cycles to yield a complete data set in accordance with ASE guidelines.1 The traditional 4-chamber LAP view was modified by placement of the probe in a more cranial position to optimize images of the right side of the heart. Image acquisition was triggered by appropriate recognition of an R wave on the simultaneous ECG tracing. Care was taken to ensure that the entire atrium was included in the 3-D pyramidal data set, and 4 wedge-shaped subvolumes were obtained for each complete cardiac cycle. Images were stored digitally and analyzed offline by use of a workstation with commercial softwaref designed for quantification of general chamber volumes. Reference points were manually placed to designate maximum atrial volume just prior to atrioventricular valve opening (Figure 3).
Each echocardiographic measurement was collectively obtained in triplicate by 2 observers (EJO and NLL), who were unaware of (blinded to) the MDCT-derived volume measurements. The mean was calculated for each measurement and used for statistical analysis.
Statistical analysis
Statistical analyses were performed with commercially available software.g Raw and indexed data were assessed for normality by use of the D'Agostino and Pearson normality test. Because of the small study population, nonparametric testing was performed.16 The median and range were reported for the LAV and RAV determined by each measurement technique. The MDCT-derived values for LAV and RAV were compared with 2DE and 3DE measurements by use of the Friedman test; MDCT measurements were considered the gold standard. The Dunnett multiple comparisons test was used to account for serial comparisons and provide adjusted P values. Raw MDCT-derived RAV and LAV measurements were compared with the Wilcoxon signed rank test and Spearman correlation coefficient. The extent of agreement between echocardiographic and MDCT measurements was evaluated by the Bland-Altman method. The bias for echocardiographic measurements relative to MDCT measurements was determined, and the corresponding SD was used to determine the 95% limits of agreement. Values of P < 0.05 were considered significant for all analyses.
Results
Raw and indexed values for LAV and RAV for all measurement techniques were summarized (Table 1). The indexed LAVs determined from 3DE (P = 0.09), 2DE LAP (P = 0.06), and 2DE RPS (P > 0.99) views did not differ significantly from those determined from MDCT images. Conversely, the indexed RAVs determined from 3DE (P < 0.001), 2DE LAP (P < 0.001), and 2DE LCR (P = 0.009) images were significantly lower than those determined from MDCT images. The MDCT-derived RAV was significantly (P = 0.024) greater than the MDCT-derived LAV by a median of 1.1 mL; however, there was a strong positive correlation (rS = 0.85) between MDCT-derived RAV and LAV measurements.
Median (range) values for LAV and RAV determined by various 2DE and 3DE methods and MDCT for 11 healthy young adult purpose-bred hound-type dogs.
Variable | Imaging method | Unindexed volume (mL) | Indexed volume (mL/kg)* |
---|---|---|---|
LAV | MDCT | 20.19 (17.43–31.77) | 1.10 (0.81–1.35) |
3DE | 18.90 (14.30–23.27) | 0.97 (0.62–1.38) | |
2DE via the LAP window | 19.70 (13.80–24.76) | 0.99 (0.79–1.21) | |
2DE via the RPS window | 22.02 (15.28–28.43) | 1.19 (0.83–1.36) | |
RAV | MDCT | 21.32 (18.24–30.94) | 1.23 (0.93–1.32) |
3DE | 14.00 (8.10–19.80) | 0.75 (0.35–1.05)† | |
2DE via the LAP window | 13.04 (8.10–19.91) | 0.64 (0.39–0.96)† | |
2DE via the LCR window | 13.91 (6.25–19.86) | 0.70 (0.37–1.09)† |
Indexed to body weight. †Within a variable and column, value differs significantly (P < 0.05) from that for the MDCT method.
Bland-Altman analyses indicated that the LAV and RAV determined by 2DE and 3DE methods were underestimated when compared with the LAV and RAV determined by MDCT (Figure 4). For the indexed LAV, the measurement determined from 2DE RPS images had the least amount of bias (−0.008 mL/kg; 95% limits of agreement, −0.36 to 0.34 mL/kg), although measurements determined from 2DE LAP (bias, −0.11 mL/kg; 95% limits of agreement, −0.42 to 0.21 mL/kg) and 3DE (bias, −0.15 mL/kg; 95% limits of agreement, −0.50 to 0.20 mL/kg) images also had minimal bias. For the indexed RAV, bias relative to the MDCT-derived measurement was pronounced for measurements determined from 3DE (−0.40 mL/kg; 95% limits of agreement, −0.77 to −0.04 mL/kg), 2DE LAP (−0.51 mL/kg; 95% limits of agreement, −0.86 to −0.16 mL/kg), and 2DE LCR (−0.43 mL/kg; 95% limits of agreement, −0.86 to 0.00 mL/kg) images.
Discussion
Results of the present study indicated that the LAV and RAV determined by 2DE and 3DE consistently underestimated the LAV and RAV determined by ECG-gated MDCT, the volumetric gold standard for atrial volume measurement used in this study. The magnitude by which echocardiographic measurements underestimated atrial volume was greater for RAV than for LAV. In fact, the LAV measurements determined by 2DE and 3DE did not differ significantly from the LAV determined by MDCT.
In the present study, bias was minimal between MDCT-derived LAV measurements and LAV measurements derived from 2DE and 3DE. The bias was smallest between the LAV determined from 2DE RPS images and that determined by MDCT. That finding was logical because the left atrium is easier to image through the RPS window than through the LAP window owing to its closer proximity to the ultrasound probe. Consequently, results suggested that the LAV determined by the MOD from 2DE images obtained via the RPS window was most similar to the LAV determined by the volumetric gold standard and, thus, the most accurate echocardiographic method for estimating LAV.
In contrast to echocardiographically derived LAV measurements, the RAVs estimated by 2DE and 3DE were significantly lower than the RAV determined by MDCT. That finding was likely the result of underestimation of the RAV by echocardiographic methods rather than overestimation of the RAV by MDCT. The disparity between echocardiographically derived and MDCT-derived RAV measurements might have been caused by technique differences (eg, cessation of spontaneous respiration during the acquisition of MDCT images), difficulty associated with adequately imaging the right atrium echocardiographically, or a combination of multiple factors. It is feasible for the RAV to be slightly greater than the LAV during full-inspiration breath holding for MDCT image acquisition. Also, visualization of the entire extent of the right atrial body through conventional echocardiographic windows is challenging. In the present study, bias relative to the MDCT-derived RAV was smallest for the RAV determined by 3DE, followed closely by that determined with 2DE LCR images. The right atrium was difficult to image with 2DE via the LAP window because, with the probe positioned at that window, the right atrium was a far-field structure, which necessitated modifying the position of the probe to visualize it. Additionally, although the right atrium is a near-field structure when echocardiographically assessed by positioning of the probe in right-sided windows (eg, RPS window), it is often incompletely visualized in the long-axis view and attempts to optimize visualization of the right atrium in that view often result in undesirable lung artifact.
Results of the present study suggested that atrial volumes derived from 3DE were not particularly robust. The median RAV determined by 3DE was significantly lower than the median RAV determined by MDCT. The median LAV determined by 3DE was also lower than the median LAV determined by MDCT, but the difference did not quite reach our cutoff for significance (P = 0.09), which we suspected was caused by a small study population and type I error. We believe that the LAV derived from 3DE would have been significantly lower than that derived by MDCT in a more robustly powered study (ie, had more dogs been evaluated). Results of multiple studies17–21 indicate that 3DE consistently underestimates the cardiac volume of healthy dogs relative to measurements obtained by a volumetric gold standard. There are several plausible explanations for that underestimation. The spatial and temporal resolutions of cMRI and MDCT are excellent and greater than those of currently available 3DE. Differences in temporal resolution can result in measurements being obtained at different points of the cardiac cycle despite efforts to consistently measure volume at ventricular end systole. The rapid injection of iodinated contrast medium during MDCT scanning could increase cardiac preload and atrial dimensions on MDCT images. Also, distinction of the myocardial border on contrast-enhanced MDCT images is superior to that achieved on echocardiographic images, which facilitates delineation of venous attachments and atrial appendages during volume calculations. Finally, ventilation may have affected atrial volume measurements. Spontaneous respiration was allowed during acquisition of echocardiographic images but not during acquisition of MDCT images.
In the present study, the MDCT-derived RAV was significantly greater than the MDCT-derived LAV by a mean of 0.06 mL/kg. Although that difference was statistically significant, its clinical relevance was nominal. For example, for a 20-kg dog with an LAV of approximately 22 mL, the RAV would be approximately 1.2 mL greater than the LAV. In healthy mammalian hearts, the RAV is expected to be almost the same as the LAV.22 The difference between the MDCT-derived RAV and LAV observed in this study might have been a consequence of the use of an inspiratory breath-hold technique during image acquisition. Alternatively, the MDCT-derived RAV might have been slightly overestimated because contrast opacification of the right atrium is nonuniform owing to unavoidable dilution and uneven mixing of the contrast medium by venous blood. Passage of the contrast medium–laden blood through the pulmonary circulation allows the contrast medium to become more evenly distributed in the blood, which results in more uniform opacification of all left atrial structures and venous attachments. Although comparison of LAV with RAV is currently lacking for veterinary species, results of a human study22 indicate that the indexed LAV is greater than the indexed RAV when measured by echocardiographic methods. That study22 also indicated that, compared with atrial volumes determined by cMRI (volumetric standard), echocardiography underestimated RAV to a greater extent than LAV. Similarly, in another human study,23 the mean ratio for echocardiographically derived atrial volume to cMRI-derived atrial volume was 0.5 for LAV and 0.46 for RAV (ie, the magnitude of underestimation by echocardiography was greater for RAV than for LAV). In the present study, the fact that the median MDCT-derived RAV was only slightly greater than the median MDCT-derived LAV suggested that the differences observed between echocardiographic atrial volume measurements were likely the result of underestimation of RAV rather than overestimation of LAV.
From a clinical standpoint, the extent of bias between echocardiographically derived and MDCT-derived RAV estimates suggested that the 2 methods should not be used interchangeably to measure RAV. However, bias was minimal between echocardiographically derived and MCDT-derived LAV estimates; thus, echocardiographic estimation of LAV might be clinically useful. Echocardiography may be clinically useful for serial monitoring of atrial volumes over time in individual patients despite its apparent propensity for underestimating those measures, particularly RAV. Furthermore, we recommend that 2DE methods be used for echocardiographic quantification of atrial size until the temporal and spatial resolutions for 3DE improve substantially. Advances in 3DE probe, machine, and software technology are expected to cumulatively improve the resolution of that modality.
The present study had several limitations. The study population was small (n = 11 dogs), and all dogs were of a similar breed, age, and weight. All dogs were also healthy. The external validity of the results of this study, especially for dogs with atrial enlargement, is unknown. Additionally, variability analysis was not performed because each dog was evaluated by a particular modality only once and measurements were collectively obtained by both an inexperienced and experienced cardiologist. The experienced cardiologist oversaw each individual measurement to minimize bias. Results of a previous study24 suggest that the magnitude of bias for 3DE-derived measurements is inversely related to the experience of the person obtaining the measurements (ie, bias is less for experienced investigators than for inexperienced investigators). Also, MDCT was performed before echocardiography for 6 of the 11 study dogs. It is possible that anesthesia may have confounded myocardial function; however, echocardiographically derived atrial volumes were consistently lower than MDCT-derived atrial volumes regardless of the sequence in which MDCT and echocardiography were performed. Finally, owing to the small study population, the data presented in this report represented results of nonparametric tests. However, all continuous variables evaluated in this study appeared to be normally distributed, and we reached the same conclusions after the data set underwent parametric testing. We believe this further validated our findings because parametric tests are more statistically robust than nonparametric tests.16
In the present study, echocardiographic determination of LAV was closely correlated with that determined by MDCT, but the same was not true for RAV. Thus, echocardiography and MDCT are not interchangeable for determination of RAV. It is important to note that this study represented a preliminary evaluation of the relationship between atrial volumes measured by echocardiography and MDCT in healthy dogs and involved the use of fairly sophisticated techniques for measurement of atrial volumes. The findings of the present study need to be validated in a larger more variable population of dogs with and without cardiac disease to delineate the exact benefits and constraints of the assessed methods.
Acknowledgments
Supported by research funds from the Department of Clinical Sciences, Carlson College of Veterinary Medicine, Oregon State University.
The authors declare that there were no conflicts of interest.
The authors thank Darcy Palmer, Amy Berry, Robyn Panico, Allison Lake, Cynthia Viramontes, and Jason Wiest for technical assistance.
ABBREVIATIONS
2DE | 2-dimensional echocardiography |
3DE | 3-dimensional echocardiography |
ASE | American Society of Echocardiography |
cMRI | Cardiac MRI |
LAP | Left apical |
LAV | Left atrial volume |
LCR | Left cranial |
MDCT | Multidetector CT |
MOD | Method of disks |
RAV | Right atrial volume |
RPS | Right parasternal |
Footnotes
Toshiba Aquilion 64 CT, Toshiba America Medical Systems Inc, Tustin, Calif.
Isovue 370, Empower CTA, Bracco Diagnostics Inc, Princeton, NJ.
Empower CTA, Bracco Diagnostics Inc, Princeton, NJ.
Vitrea workstation software, version 6.7.4, Vital Images Inc, Minnetonka, Minn.
iE33, Philips Medical Systems, Andover, Mass.
TomTec Imaging Systems GmbH, Munich, Germany.
Prism, version 6.0h, GraphPad Software Inc, La Jolla, Calif.
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