• View in gallery

    Left ventricular tissue velocity data obtained from a right parasternal tissue Doppler echocardiographic short-axis view at the papillary muscle level in a horse. On the image, caudal is to the right. On the left side of the figure, the TDI color cineloop and a grayscale cineloop are displayed, revealing the sample area positions for LVFW (yellow) and IVS (green). On the right, segmental traces are displayed for LVFW (yellow) and IVS (green). The x-axis indicates time (milliseconds), over which is superimposed the ECG. The y-axis indicates tissue velocity (cm/s). Peak values (IVC, Syst, IVR, E, and A) and time intervals (PEP, EET, and duration A) are indicated on the LVFW curve.

  • View in gallery

    Left ventricular strain rate data obtained from a right parasternal tissue Doppler echocardiographic short-axis view at the papillary muscle level in a horse. The y-axis indicates strain rate (s−1). See Figure 1 for remainder of key.

  • View in gallery

    Left ventricular strain data obtained from a right parasternal tissue Doppler echocardiographic short-axis view at the papillary muscle level in a horse. The y-axis indicates strain (%). Peak values (St syst and St max) are indicated on the LVFW and IVS curves. See Figure 1 for remainder of key.

  • View in gallery

    Left ventricular tissue velocity data obtained from a left parasternal tissue Doppler echocardiographic short-axis view at the chordal level in a horse. On the image, cranial is to the right. On the left side of the figure, the TDI color cineloop and a grayscale cineloop are displayed, revealing the sample area positions for LLV (yellow) and RLV (green). On the right, segmental traces are displayed for LLV (yellow) and RLV (green). The y-axis indicates tissue velocity (cm/s). See Figure 1 for remainder of key.

  • View in gallery

    Left ventricular strain rate data obtained from a left parasternal tissue Doppler echocardiographic short-axis view at chordal level in a horse. On the image, cranial is to the right. On the left side of the figure, the TDI color cineloop and a grayscale cineloop are displayed, revealing the sample area positions for LLV (yellow) and RLV (green). On the right, segmental traces are displayed for LLV (yellow) and RLV (green). The y-axis indicates strain rate (s−1). See Figure 1 for remainder of key.

  • View in gallery

    Left ventricular strain rate data obtained from a left parasternal tissue Doppler echocardiographic short-axis view at chordal level in a horse. The y-axis indicates the strain (%). Peak values (St syst and St max) are indicated on the LLV and RLV curves. See Figures 1 and 5 for remainder of key

  • View in gallery

    Illustration of measurements performed on an LVFW tissue velocity curve obtained from a right parasternal tissue Doppler echocardiographic short-axis view at the chordal level in a horse. The peak R wave and onset P wave on the ECG are indicated by blue dotted lines. The y-axis indicates tissue velocity (cm/s). Peak values (IVC, Syst, IVR, E, and A) are indicated by yellow arrows and yellow labels. Time measurements (tIVC, PEP, tSyst, EET, tIVR, onset E, tE, onset A, tA, and duration A) are indicated by white arrows and white labels. See Figure 1 for remainder of key.

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Evaluation of tissue Doppler imaging for regional quantification of radial left ventricular wall motion in healthy horses

Annelies Decloedt DVM, PhD1, Tinne Verheyen DVM, PhD2, Stanislas Sys MD, PhD3, Dominique De Clercq DVM, PhD4, and Gunther van Loon DVM, PhD5
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  • 1 Department of Large Animal Internal Medicine, Faculty of Veterinary Medicine, Ghent University, 9820 Merelbeke, Belgium.
  • | 2 Department of Large Animal Internal Medicine, Faculty of Veterinary Medicine, Ghent University, 9820 Merelbeke, Belgium.
  • | 3 Department of Large Animal Internal Medicine, Faculty of Veterinary Medicine, Ghent University, 9820 Merelbeke, Belgium.
  • | 4 Department of Large Animal Internal Medicine, Faculty of Veterinary Medicine, Ghent University, 9820 Merelbeke, Belgium.
  • | 5 Department of Large Animal Internal Medicine, Faculty of Veterinary Medicine, Ghent University, 9820 Merelbeke, Belgium.

Abstract

Objective—To compare the feasibility and repeatability of tissue Doppler imaging (TDI) for quantification of radial left ventricular (LV) velocity and deformation from different imaging planes and to correlate cardiac event timing data obtained by TDI to M-mode and pulsed-wave Doppler-derived time intervals in horses.

Animals—10 healthy adult horses.

Procedures—Repeated echocardiography was performed by 2 observers from right and left parasternal short-axis views at papillary muscle and chordal levels. The TDI measurements of systolic and diastolic velocity, strain rate, strain peak values, and timing were performed in 8 LV wall segments (LV free wall and interventricular septum from right parasternal views; left and right region of LV wall from left parasternal views). The inter- and intraobserver within- and between-day variability and measurement variability were assessed. The correlation between TDI-based measurements and M-mode and pulsed-wave Doppler-based time measurements was calculated.

Results—TDI measurements of velocity, strain rate, and strain were feasible in each horse, although deformation could often not be measured in the LV free wall. Systolic and diastolic time intervals could be determined with low to moderate variability, whereas peak amplitude variability ranged from low to high. The TDI-based time measurements were significantly correlated to M-mode and pulsed-wave Doppler measurements.

Conclusions and Clinical Relevance—TDI measurements of radial LV velocity and deformation were feasible with low to moderate variability in 8 LV segments. These measurements can be used for evaluating LV function in further clinical studies.

Abstract

Objective—To compare the feasibility and repeatability of tissue Doppler imaging (TDI) for quantification of radial left ventricular (LV) velocity and deformation from different imaging planes and to correlate cardiac event timing data obtained by TDI to M-mode and pulsed-wave Doppler-derived time intervals in horses.

Animals—10 healthy adult horses.

Procedures—Repeated echocardiography was performed by 2 observers from right and left parasternal short-axis views at papillary muscle and chordal levels. The TDI measurements of systolic and diastolic velocity, strain rate, strain peak values, and timing were performed in 8 LV wall segments (LV free wall and interventricular septum from right parasternal views; left and right region of LV wall from left parasternal views). The inter- and intraobserver within- and between-day variability and measurement variability were assessed. The correlation between TDI-based measurements and M-mode and pulsed-wave Doppler-based time measurements was calculated.

Results—TDI measurements of velocity, strain rate, and strain were feasible in each horse, although deformation could often not be measured in the LV free wall. Systolic and diastolic time intervals could be determined with low to moderate variability, whereas peak amplitude variability ranged from low to high. The TDI-based time measurements were significantly correlated to M-mode and pulsed-wave Doppler measurements.

Conclusions and Clinical Relevance—TDI measurements of radial LV velocity and deformation were feasible with low to moderate variability in 8 LV segments. These measurements can be used for evaluating LV function in further clinical studies.

Tissue Doppler imaging is increasingly used in veterinary cardiology to evaluate LV function. Tissue Doppler imaging allows quantification of systolic and diastolic myocardial velocities on the basis of the Doppler principle. Conventional color flow Doppler imaging measures the high-velocity, low-intensity signals from the blood pool by use of high-pass filtering. In contrast, TDI captures the low-velocity, high-intensity myocardial signals by use of a low-pass filter.1 A limitation of the Doppler principle is that measurements are restricted to the direction of the ultrasonographic beam. Because the acquisition of apical images is impossible in adult horses, only radial myocardial velocity and deformation can be assessed by use of parasternal images. Deformation indices are calculated on the basis of the myocardial velocity gradient from the endocardium to the epicardium.2 Strain is defined as the total amount of myocardial deformation, expressed as a percentage relative to the end-diastolic wall thickness. The change in strain per time unit is the strain rate, expressed in s−1.

In small animals, the reliability of TDI and its use for early detection of impaired contractility in cardiomyopathy have been extensively described.3–5 In equine cardiology, the feasibility and reliability of TDI have been studied in healthy horses at rest and after exercise.6–8 In a horse with nutritional masseter myodegeneration, systolic and diastolic myocardial dysfunction could be quantified by pulsed-wave TDI.9 However, the reliability of TDI measurements in horses has been assessed in only 1 LV free wall segment from a right parasternal short-axis view.7 In that study,7 deformation indices revealed poor repeatability. It is unknown whether the use of other segments and left parasternal views might allow strain and strain rate measurements in horses. Furthermore, TDI allows accurate timing of cardiac events because of the high frame rate. However, the relationship between TDI-based and M-mode or pulsed-wave Doppler-based timings has not been studied in horses yet.

The purpose of the study reported here was to compare the feasibility and repeatability of TDI for quantification of myocardial velocity and deformation in 8 LV wall segments from right and left parasternal short-axis views at the papillary muscle and chordal levels in horses. Cardiac event timing evaluated by TDI was compared with that obtained by M-mode and pulsed-wave Doppler techniques.

Materials and Methods

Echocardiography—Ten healthy untrained French Trotters (mean ± SD age, 9.6 ± 4.4 years; body weight, 509 ± 58 kg; 7 mares and 3 geldings) were examined at heart rates < 45 beats/min via an ultrasonographic unita and phased-array transducerb at a frequency of 1.7/3.4 MHz. A base-apex ECG was recorded simultaneously. All procedures were approved by the Ethical Committee, Faculty of Veterinary Medicine, Ghent University, and animal handling and care were performed following their guidelines. Right parasternal LV outflow tract M-mode recordings were made for timing of aortic valve opening and closure by M-mode. Pulsed-wave Doppler measurements of aortic outflow were obtained from the left parasternal position. Mitral valve motion was assessed from a right parasternal short-axis M-mode image. For color-coded tissue Doppler images, the grayscale width was reduced to 30° and the TDI sector was narrowed to the smallest effective region of interest. The velocity scale was set from 32 to −32 cm/s, resulting in a frame rate of 183 frames/s. Right and left parasternal short-axis views were acquired at the papillary muscle and chordal levels. The probe was always turned counterclockwise so that right on the screen was caudal for the right parasternal short-axis views and cranial for the left parasternal views. The image orientation was optimized for parallel alignment of radial wall motion to the ultrasonographic beam. The echocardiographic recordings were digitally stored as cineloops for subsequent offline analyses.

Determination of M-mode and pulsed-wave Doppler indices—All offline measurements were performed with dedicated software.c The aortic valve opening M-mode, aortic valve opening and closure M-mode, and mitral valve opening M-mode were measured as the time interval between the peak R wave on the ECG and valve opening or closure in the M-mode image. Timing of aortic valve opening and closure by pulsed wave and aortic valve closure pulsed wave was measured as the time interval between the R wave and onset or end of aortic flow. The mean of 3 nonconsecutive cycles was used for further analysis.

Determination of TDI indices—Loops of 3 consecutive cycles were analyzed with the Q-analysis mode of the software. The IVS and LVFW were evaluated from right parasternal views. From the left parasternal imaging planes, LLV and RLV were assessed.6 The positions of sample areas in each segment are illustrated (Figures 1–6). Sample area length (12 to 17 mm) and width (5 to 6 mm) were adapted to wall thickness. The sample area was anchored inside the myocardium by use of the software available in the workstation.c This facilitated tracking of the motion of the myocardial segments during the cardiac cycle. The sample area was set to the mid-myocardium at the time of peak R on the ECG and at the end of systole, early diastole, diastasis, and atrial contraction.

Figure 1—
Figure 1—

Left ventricular tissue velocity data obtained from a right parasternal tissue Doppler echocardiographic short-axis view at the papillary muscle level in a horse. On the image, caudal is to the right. On the left side of the figure, the TDI color cineloop and a grayscale cineloop are displayed, revealing the sample area positions for LVFW (yellow) and IVS (green). On the right, segmental traces are displayed for LVFW (yellow) and IVS (green). The x-axis indicates time (milliseconds), over which is superimposed the ECG. The y-axis indicates tissue velocity (cm/s). Peak values (IVC, Syst, IVR, E, and A) and time intervals (PEP, EET, and duration A) are indicated on the LVFW curve.

Citation: American Journal of Veterinary Research 74, 1; 10.2460/ajvr.74.1.53

Figure 2—
Figure 2—

Left ventricular strain rate data obtained from a right parasternal tissue Doppler echocardiographic short-axis view at the papillary muscle level in a horse. The y-axis indicates strain rate (s−1). See Figure 1 for remainder of key.

Citation: American Journal of Veterinary Research 74, 1; 10.2460/ajvr.74.1.53

Figure 3—
Figure 3—

Left ventricular strain data obtained from a right parasternal tissue Doppler echocardiographic short-axis view at the papillary muscle level in a horse. The y-axis indicates strain (%). Peak values (St syst and St max) are indicated on the LVFW and IVS curves. See Figure 1 for remainder of key.

Citation: American Journal of Veterinary Research 74, 1; 10.2460/ajvr.74.1.53

Figure 4—
Figure 4—

Left ventricular tissue velocity data obtained from a left parasternal tissue Doppler echocardiographic short-axis view at the chordal level in a horse. On the image, cranial is to the right. On the left side of the figure, the TDI color cineloop and a grayscale cineloop are displayed, revealing the sample area positions for LLV (yellow) and RLV (green). On the right, segmental traces are displayed for LLV (yellow) and RLV (green). The y-axis indicates tissue velocity (cm/s). See Figure 1 for remainder of key.

Citation: American Journal of Veterinary Research 74, 1; 10.2460/ajvr.74.1.53

Figure 5—
Figure 5—

Left ventricular strain rate data obtained from a left parasternal tissue Doppler echocardiographic short-axis view at chordal level in a horse. On the image, cranial is to the right. On the left side of the figure, the TDI color cineloop and a grayscale cineloop are displayed, revealing the sample area positions for LLV (yellow) and RLV (green). On the right, segmental traces are displayed for LLV (yellow) and RLV (green). The y-axis indicates strain rate (s−1). See Figure 1 for remainder of key.

Citation: American Journal of Veterinary Research 74, 1; 10.2460/ajvr.74.1.53

Figure 6—
Figure 6—

Left ventricular strain rate data obtained from a left parasternal tissue Doppler echocardiographic short-axis view at chordal level in a horse. The y-axis indicates the strain (%). Peak values (St syst and St max) are indicated on the LLV and RLV curves. See Figures 1 and 5 for remainder of key

Citation: American Journal of Veterinary Research 74, 1; 10.2460/ajvr.74.1.53

The software displayed segmental velocity, strain rate, and strain curves. A 30-millisecond temporal smoothing filter was applied. Strain was calculated over a strain length or offset distance of 12 mm. Linear drift compensation was used to correct strain drift throughout the entire cardiac cycle, on the basis of the assumption that drift is linearly distributed during the cardiac cycle. As such, the strain curve always returned to zero at end diastole. The cine compound function was used to convert the last cycle into the mean of the 3 consecutive cycles. Measurements were made in this cycle. Segmental velocity and strain rate peak values and timing were measured during IVC, Syst, IVR, E, and A (Figures 1–7). The IVC was defined as the highest peak value occurring between the R wave on the ECG and the onset of Syst in the velocity and strain rate TDI curves. The IVR was defined as the highest peak value occurring between the end of Syst and onset of E in the velocity and strain rate TDI curves. All late diastolic timings were related to the onset of the preceding P wave, and all others to the peak R wave. The onset and end of systole in the tissue velocity and strain rate curves, relative to the peak R wave, were defined as PEP and EET. Onset of E, relative to the peak R wave, and A, relative to the onset of the P wave, was measured, and duration A was calculated as end A – onset A. In the strain curve, St syst and St max peak strain and timing relative to the peak R wave were measured. The St syst and St max were the same if only 1 peak was present in the strain curve. In 35% of the curves, a double strain peak was present with a second and higher peak after the end of systole. The first peak was then identified as the systolic peak strain, and the second peak was identified as the maximal peak strain.

Figure 7—
Figure 7—

Illustration of measurements performed on an LVFW tissue velocity curve obtained from a right parasternal tissue Doppler echocardiographic short-axis view at the chordal level in a horse. The peak R wave and onset P wave on the ECG are indicated by blue dotted lines. The y-axis indicates tissue velocity (cm/s). Peak values (IVC, Syst, IVR, E, and A) are indicated by yellow arrows and yellow labels. Time measurements (tIVC, PEP, tSyst, EET, tIVR, onset E, tE, onset A, tA, and duration A) are indicated by white arrows and white labels. See Figure 1 for remainder of key.

Citation: American Journal of Veterinary Research 74, 1; 10.2460/ajvr.74.1.53

Repeatability of echocardiographic variables—The repeatability of TDI measurements was evaluated by comparing repeated echocardiographic examinations and offline measurements performed by 2 experienced echocardiographers (AD and GvL). All horses were examined by observer 1 on 2 days, with a 1-day interval between observations. On one of these occasions, the examination was repeated by observer 2 immediately before or after observer 1. Offline analysis was first performed by observer 1 for all examinations (n = 30). Next, on 1 examination of each horse (n = 10), the same 3 consecutive cycles were measured by both observers on a separate occasion. Observers were unaware at all times of the identity of the echocardiographer, horse, day, or any previous results.

Statistical analysis—Statistical analyses were performed with dedicated software.d Reference values (mean ± SD; n = 10 horses) were calculated on the basis of pooled measurements of all examinations for each horse. Within-day interobserver variability was obtained by comparing the results of the echocardiographic examinations performed on the same day by observers 1 and 2, both measured by observer 1, in a 1-way repeated-measures ANOVA with horse as the unit of repeated measure. The numeric values for the reported CV were calculated by dividing the square root of the mean square error by the grand mean, then multiplying by 100%. Similarly, between-day intraobserver variability was determined by comparing the examinations recorded on 2 days by observer 1. Measurement variability was obtained by comparing the results of repeated offline measurements of 1 examination/horse on 2 days (intraobserver measurement variability) or by 2 observers (interobserver measurement variability). The degree of repeatability was defined on the basis of the CV (CV < 15%, low variability; CV 15% to 25%, moderate variability; CV > 25%, high variability).10

Measurements from different segments and views were compared by use of a linear mixed model, with segment and view as fixed categorical effects and with the horses as subjects in a repeated-measurements analysis. Agreement between conventional and TDI-based timings was assessed by simple linear regression. The difference between time to St max and aortic valve closure pulsed wave was calculated to evaluate postsystolic motion, defined as peak strain occurring after the end of ejection. For all comparisons, a value of P < 0.05 was considered significant.

Results

The TDI curves could be obtained in each segment from all views at a frame rate of 183 frames/s. Peak values and timing could be easily identified in most curves. The isovolumic peaks IVC and IVR were often absent. At papillary muscle and chordal levels, IVC was most often absent in the velocity curves of IVS and the velocity and strain rate curves of RLV. The IVR in all segments was more often absent at the chordal level, compared with the papillary muscle level. Furthermore, some peaks could not be identified due to inadequate curve quality. This mainly affected strain rate and strain in LVFW, which could frequently not be measured. As a result, the CV of these measurements could not be calculated.

Mean peak values and timing in the 8 LV segments were determined (Tables 1–4). In all velocity and strain rate curves, peak E was higher than Syst. The velocity E:A ratio in LVFW, RLV, and LLV was highly variable but was always > 1.0 in all horses. In the IVS and RLV velocity curves, the A wave was biphasic, consisting of both a negative and a positive peak velocity. In the IVS at the chordal level, the positive peak that was measured as A was often absent. Segmental timing differences were present. In the tissue velocity curves, PEP and EET were significantly (P < 0.001) shorter in IVS. In contrast, the strain rate PEP and EET measurements had no segmental differences except for shorter PEP in IVS and RLV at the chordal level (P = 0.005). Time to peak E velocity and strain rate was longer in IVS (P = 0.016) and at the papillary, compared with the chordal level (P < 0.001). Onset A occurred earlier in IVS and RLV at both levels in the velocity curves (P < 0.001). Peak strain occurred later in IVS and RLV at the chordal level (P < 0.001).

Table 1—

Mean, SD, and CV of TDI measurements of LV function from a right parasternal short-axis view at the chordal level in 10 healthy adult horses.

 LVFWIVS
 MeanSDnCVbdCVwdCVdmCVomMeanSDnCVbdCVwdCVdmCVom
Tissue velocity
 IVC (cm/s)5.35*1.84733.928.89.59.2−3.66*1.54015.626.413.312.1
 tIVC (ms)38*74720.526.07.85.631*154040.145.212.210.8
 PEP (ms)101194911.97.94.35.864*154120.130.66.45.5
 Syst (cm/s)7.391.2507.914.810.25.5−4.26*1.35021.528.95.65.3
 tSyst (ms)215425030.718.123.011.8118235014.026.121.54.6
 EET (ms)53127494.54.71.41.247534483.24.12.63.2
 IVR (cm/s)−5.13*1.64117.929.413.45.03.11*1.84538.933.111.712.7
 tIVR (ms)57031414.24.31.42.053624453.13.02.40.7
 Onset E (ms)60233413.94.51.31.562825503.43.21.41.3
 E (cm/s)−19.19*3.4507.523.711.28.112.69*2.75012.618.79.18.7
 tE (ms)68934502.93.70.60.772727502.82.51.60.8
 Onset A (ms)137*195021.423.24.83.877*155032.742.212.711.6
 A (cm/s)−7.20*2.75025.827.88.16.83.343.535NANANANA
 tA (ms)217175013.613.92.82.52123435NANANANA
 Duration A (ms)144*135013.916.46.85.5169*405015.616.410.25.9
Strain rate
 IVC (s−1)1.110.630NANANANA0.88*0.34721.627.815.012.5
 tIVC (ms)431730NANANANA23*94734.745.615.014.4
 PEP (ms)991729NANANANA81135013.614.16.75.5
 Syst (s−1)1.940.430NANANANA1.23*0.25011.515.37.09.0
 tSyst (ms)2314830NANANANA182305011.333.115.424.5
 EET (ms)5143629NANANANA51125483.24.31.20.5
 IVR (s−1)−1.510.825NANANANA−0.710.44288.978.531.910.9
 tIVR (ms)5423325NANANANA53726424.44.81.40.9
 Onset E (ms)5983126NANANANA62028502.52.91.60.6
 E (s−1)−4.740.529NANANANA−3.00*0.75014.017.713.38.7
 tE (ms)6833829NANANANA70930503.42.61.20.9
 Onset A (ms)1262629NANANANA118*255031.427.66.27.1
 A (s−1)−1.900.629NANANANA−1.24*0.55036.433.510.512.4
 tA (ms)2043629NANANANA19726509.712.94.65.9
 Duration A (ms)1581829NANANANA150*175021.826.07.96.7
Strain
 St syst (%)74.316.230NANANANA44.7*7.95018.418.85.47.3
 tSt syst (%)5213430NANANANA50926502.84.01.00.8
 St max (%)74.616.130NANANANA49.6*6.35015.518.87.28.6
 tSt max (ms)5313430NANANANA58936508.67.54.31.1

CVdm and CVom < 15%.

All CVs < 15%.

CVbd = CV of between-day intraobserver variability. CVdm = CV of intraobserver measurement variability. CVom = CV of interobserver measurement variability. CVwd = CV of within-day interobserver variability. n = Number of measurements. NA = Not available due to numerous missing values.

Table 2—

Mean, SD, and CV of TDI measurements of LV function from a right parasternal short-axis view at the papillary muscle level in horses.

 LVFWIVS
 MeanSDnCVbdCVwdCVdmCVomMeanSDnCVbdCVwdCVdmCVom
Tissue velocity
 IVC (cm/s)4.481.84935.430.715.016.2−4.29*2.14118.133.04.67.8
 tIVC (ms)41*114924.616.79.612.943*154164.348.17.44.7
 PEP (ms) 265012.87.46.67.885*314734.025.98.98.6
 Syst (cm/s)5.88*0.85018.613.310.811.2−4.49*1.25013.817.46.75.9
 tSyst (ms)238545017.124.626.024.1129*195031.914.69.33.7
 EET (ms) 26502.23.21.11.2 32503.75.51.41.7
 IVR (cm/s)−5.402.05029.931.117.520.85.262.25038.435.429.522.9
 tIVR (ms)58733504.13.61.21.455324501.82.83.31.9
 Onset E (ms)64730505.84.31.10.964430493.85.41.70.7
 E (cm/s)−13.74*1.75021.419.26.77.013.022.75023.721.216.814.9
 tE (ms)73127504.03.11.51.1 25503.33.10.80.8
 Onset A (ms)14126507.67.55.04.479*145025.526.214.07.4
 A (cm/s)−7.182.55026.325.315.411.53.563.23953.438.719.919.0
 tA (ms) 29507.19.62.92.6 44396.15.55.84.2
 Duration A (ms)142*155016.915.88.56.5189*435024.024.57.110.5
Strain rate
 IVC (s−1)0.960.329NANANANA0.83*0.24630.528.79.712.7
 tIVC (ms)411029NANANANA25144645.842.523.925.3
 PEP (ms)1061933NANANANA101225012.612.82.45.1
 Syst (s−1)1.620.636NANANANA1.260.25010.814.15.75.8
 tSyst (ms)2186536NANANANA213*435036.940.714.16.3
 EET (ms)5282534NANANANA 21503.23.71.21.8
 IVR (s−1)−1.460.629NANANANA−1.400.55051.950.09.846.6
 tIVR (ms)5793029NANANANA55522503.73.90.90.9
 Onset E (ms)6382728NANANANA 23504.85.51.90.8
 E (s−1)−3.841.030NANANANA−3.200.75013.316.413.916.8
 tE (ms)7163130NANANANA 23504.64.11.71.7
 Onset A (ms)1221933NANANANA136*345037.622.16.65.5
 A (s−1)−1.540.533NANANANA−1.51*0.95034.250.14.46.8
 tA (ms)2072033NANANANA 28509.810.44.13.9
 Duration A (ms)1552333NANANANA138*285030.027.912.912.8
Strain
 St syst (%)54.713.235NANANANA43.3*7.15016.019.06.27.1
 tSt syst (%)5302735NANANANA 21503.53.51.01.1
 St max (%)54.813.235NANANANA44.4*6.05016.419.16.07.2
 tSt max (ms)5422335NANANANA559555011.212.21.51.1

See Table 1 for key.

Table 3—

Mean, SD, and CV of TDI measurements of LV function from a left parasternal short–axis view at the chordal level in horses.

 LLVRLV
 MeanSDnCVbdCVwdCVdmCVomMeanSDnCVbdCVwdCVdmCVom
Tissue velocity
 IVC (cm/s)−3.602.95044.344.118.213.08.05*2.84714.618.18.810.3
 tIVC (ms)46105014.811.38.49.458*10479.718.16.15.8
 PEP (ms)106165010.513.73.92.1133*324821.115.76.36.1
 Syst (cm/s)−4.631.55015.016.99.016.9 0.6509.48.94.84.9
 tSyst (ms)319725022.015.618.710.6208*285016.78.06.43.3
 EET (ms) 31502.54.21.11.5 33505.06.11.42.3
 IVR (cm/s)2.531.04757.950.019.919.1−3.151.34536.036.218.313.5
 tIVR (ms)55939473.24.91.21.155838452.94.12.23.2
 Onset E (ms)61047503.44.31.71.559532503.24.51.92.6
 E (cm/s)13.521.65014.923.724.618.9−18.44*1.85016.218.812.814.4
 tE (ms) 44503.83.50.92.2 37503.84.01.51.5
 Onset A (ms)130215016.616.717.916.279*274952.230.814.113.2
 A (cm/s)2.481.25051.543.016.513.1−1.880.64828.728.614.514.3
 tA (ms)21417509.610.611.210.4150214818.019.34.65.3
 Duration A (ms)148175011.212.610.25.6218*234915.612.84.96.5
Strain rate
 IVC (s−1)1.631.24939.138.218.120.30.570.326NANANANA
 tIVC (ms)43*84917.131.510.66.3331226NANANANA
 PEP (ms)100*154910.421.46.45.688*164813.015.311.313.7
 Syst (s−1) 0.45012.210.17.412.11.49*0.25015.59.75.64.9
 tSyst (ms)291*515020.227.810.511.0294365031.831.227.425.7
 EET (ms) 30504.26.92.42.7 42504.15.12.93.3
 IVR (s−1)−0.890.632NANANANA−0.530.434NANANANA
 tIVR (ms)5533932NANANANA5494334NANANANA
 Onset E (ms) 39464.86.21.21.8 38483.56.42.71.5
 E (s−1)−5.94*1.45017.118.712.014.3−5.290.84929.420.823.516.6
 tE (ms) 45503.84.81.52.5 41492.64.71.42.2
 Onset A (ms)114*185018.514.44.16.2107*304943.524.69.514.4
 A (s−1)−1.700.45040.526.729.416.0−1.360.54940.318.729.714.1
 tA (ms)202275012.212.112.212.1179*284921.318.27.66.2
 Duration A (ms)16912509.87.16.96.4143*194920.014.17.213.8
Strain
 St syst (%)107.4*20.35018.714.512.712.762.3*9.55017.316.111.88.2
 tSt syst (%) 28503.16.82.91.8 33503.85.62.03.0
 St max (%)110.0*18.05018.512.612.512.169.2*9.55017.815.312.79.1
 tSt max (ms)55639504.66.32.93.360533507.57.82.92.2

See Table 1 for key.

Table 4—

Mean, SD, and CV of TDI measurements of LV function from a left parasternal short-axis view at the papillary muscle level in horses.

 LLVRLV
 MeanSDnCVbdCVwdCVdmCVomMeanSDnCVbdCVwdCVdmCVom
Tissue velocity
 IVC (cm/s)−5.42*3.05025.827.112.412.15.52*3.54247.921.78.77.1
 tIVC (ms)40*85025.632.111.210.847*214238.719.67.014.1
 PEP (ms) 165011.411.63.93.2126*414520.519.63.45.6
 Syst (cm/s)−4.431.45019.715.318.611.54.69*0.75020.419.46.98.4
 tSyst (ms)211425038.832.123.738.7215*455028.929.88.02.8
 EET (ms) 32504.34.82.71.1 34504.04.31.91.6
 IVR (cm/s)3.511.05033.249.528.016.3−3.641.74516.429.541.314.9
 tIVR (ms)56635505.45.04.21.057138453.33.92.12.9
 Onset E (ms)65153504.75.01.62.361032454.04.92.02.7
 E (cm/s)9.00*3.55029.122.014.312.0−13.60*2.65025.614.612.914.5
 tE (ms) 50505.04.21.71.3 38503.84.02.32.4
 Onset A (ms)126*235017.313.112.114.481195036.639.724.639.4
 A (cm/s)4.201.15030.120.414.823.3−1.330.54535.446.25.821.2
 tA (ms)220255012.97.62.54.3144244520.822.97.67.2
 Duration A (ms)160135012.09.68.78.3222*245015.111.810.611.4
Strain rate
 IVC (s−1)2.001.05037.449.812.216.01.400.64023.618.413.522.0
 tIVC (ms)39*95030.032.511.88.438144017.236.85.017.7
 PEP (ms)94*195016.718.59.49.899*194423.712.87.98.7
 Syst (s−1)2.28*0.35012.420.88.811.61.29*0.34513.217.07.611.1
 tSyst (ms)220465017.346.925.631.2272644526.642.130.537.0
 EET (ms) 31503.84.52.11.5 31454.63.52.82.3
 IVR (s−1)−1.910.94746.630.533.131.1−1.420.64458.918.326.217.4
 tIVR (ms)56640475.14.55.02.955839444.73.33.22.7
 Onset E (ms)63149474.85.92.92.664347456.24.91.91.8
 E (s−1)−3.770.75020.921.721.018.3−4.341.04536.318.231.634.6
 tE (ms) 56506.36.13.42.7 48456.04.51.92.6
 Onset A (ms)112215019.718.017.818.5123*274435.923.411.613.0
 A (s−1)−2.140.65021.426.010.621.8−0.970.34450.530.017.421.3
 tA (ms)20823506.19.214.46.2 254413.014.43.95.6
 Duration A (ms)169135011.310.58.810.3130334413.110.37.719.5
Strain
 St syst (%)93.6*14.25021.222.57.411.551.8*134515.816.75.88.7
 tSt syst (%) 28504.34.42.01.2 30454.52.92.21.7
 St max (%)93.7*14.25021.122.57.411.553.3*12.04513.915.76.38.5
 tSt max (ms)51427505.44.42.01.253445456.22.95.44.7

See Table 1 for key.

Table 5—

Mean, SD, minimum, and maximum of the difference between time to St max measured by TDI and aortic valve opening and closure by pulsed wave.

  St max – aortic valve closure pulsed wave (ms)
Imaging planeSegmentMeanSDRange
Right short-axis chordal levelLV−940−82 to 96
 IVS5455−96 to 154
Right short-axis papillary levelLV−533−76 to 83
 IVS2467−51 to 160
Left short-axis chordal levelLLV2045−53 to 112
 RLV6941−29 to 165
Left short-axis papillary levelLLV−2121−53 to 53
 RLV−446−62 to 116

Compared with M-mode and pulsed-wave Doppler measurements, EET measured in the velocity and strain rate curves of the different segments was significantly correlated to aortic valve closure M-mode (r = 0.54 to 0.80; P < 0.05) and aortic valve closure pulsed wave (r = 0.54 to 0.89; P < 0.05), except for strain rate in LVFW. Similarly, onset E was significantly correlated with mitral valve opening M-mode (r = 0.45 to 0.83; P < 0.01). The PEP was only moderately correlated with aortic valve opening M-mode and aortic valve opening pulsed wave. In the segments with significant correlations, r ranged from 0.39 to 0.59 and 0.38 to 0.58, respectively. The difference between time to St max and aortic valve opening and closure by pulsed wave was tabulated (Table 5). Postsystolic motion was mainly present in the IVS and RLV at the chordal level.

Variability of the TDI measurements was noted (Tables 1–4). Variability was low for most systolic and diastolic timing measurements but ranged from low to high for peak values. However, for several peak values, between-day intraobserver and within-day interobserver variability were moderate to high, whereas measurement variability was low.

Discussion

Results of this study indicated the feasibility and repeatability of color-coded TDI for quantification of radial wall motion in 8 LV segments from right and left parasternal short-axis images at the papillary muscle and chordal levels in horses. Myocardial velocity and deformation could be measured easily in all segments except for strain rate and strain in the LV free wall from right parasternal views. Peak values had higher variability, compared with timing measurements. Time measurements by TDI correlated with M-mode and pulsed-wave Doppler-based measurements.

The tissue velocity and strain rate curves revealed 3 major deflections: 1 during systole (Syst) and 2 during diastole (E and A). The IVC and IVR were smaller, often biphasic, and had a short duration, which made these peaks rather difficult to identify. The IVC and IVR were also frequently absent, which might have been caused by smoothing of the curves with the cine compound function. The numeric values of peak amplitudes and timing measured in the LVFW at the chordal level were similar to those found by Schwarzwald et al.7 The peak amplitudes measured in IVS, LLV, and RLV at the chordal level were generally equal to or lower than those described by Sepulveda et al.6 The velocity E:A ratio was > 1.0 in all horses, as described in healthy dogs.3 Impaired LV relaxation in the early stages of diastolic dysfunction causes prolonged isovolumic relaxation time, reduced early filling, and increased dependence on atrial contraction, resulting in E:A ratio < 1. In human medicine, this can be easily assessed by pulsed-wave transmitral flow measurements.11 In horses, these measurements are highly variable due to poor alignment, and TDI might be an easier alternative to assess diastolic function. In a horse with nutritional masseter myopathy, diastolic dysfunction could be detected both by TDI and transmitral flow Doppler ultrasonography.9

Strain rate and strain could be measured in all segments except LVFW, which was probably caused by the image depth of this segment. Strain rate and strain offer several advantages over velocity measurements. A noncontractile myocardial segment will have no intrinsic active deformation, whereas wall motion because of tethering by the adjacent segments can be present. As a result, myocardial velocities can be close to reference range, whereas strain rate and strain curves are altered.12 Furthermore, deformation indices are not affected by total heart motion.13 The possible advantages of TDI-based deformation indices in horses with cardiac disease require further investigation. A limitation of TDI strain and strain rate measurements is the angle dependency. Only radial strain can be measured by use of parasternal images. In contrast, 2-D speckle tracking is an angle-independent technique that measures myocardial wall motion on the basis of tracking speckles in the 2 dimensions of the ultrasonographic image. This allows quantification of radial, circumferential, and longitudinal strain. However, the frame rate used for 2-D speckle tracking is much lower.

Because of the high frame rate (> 180 frames/s), TDI allows accurate time measurements. A good correlation between systolic and diastolic time intervals measured by TDI and by invasive hemodynamics has been reported in human medicine.14 In the present study, TDI-based measurements of PEP, EET, and onset E correlated with M-mode and pulsed-wave Doppler measurements. Correlation was better for EET and onset E than for PEP. Because PEP is short, the measurement error of all methods is relatively large. Furthermore, TDI-based and conventional measurements were made in different cycles, thereby adding physiologic variability of heart rate and inotropy. The main advantage of TDI is that systolic and diastolic time intervals can be acquired from 1 image. In the horse with nutritional masseter myopathy and myocardial damage, an increased ratio of PEP:ejection time and a longer isovolumic relaxation time could be measured by TDI, indicating both systolic and diastolic dysfunction.9

However, significant segmental differences of peak timing were present. Differences were mainly found in the velocity curves, which was probably due to total heart motion and interaction with right ventricular motion. The earlier onset of velocity peak A in IVS and RLV is caused by the delay in left, compared with right atrial activation. This also explains the biphasic shape of the A wave. Strain rate timing measurements had less segmental differences in these healthy horses at resting heart rate, indicating a synchronous contraction pattern. The longer time to peak strain found in IVS and RLV at the chordal level was similar to the delayed peak longitudinal strain in the basal septal segment measured by 2-D speckle tracking15 because RLV is located at the transition of the septum and LV free wall. The clinical importance of the observed postsystolic motion in healthy horses is unknown. A double peak with postsystolic St max was present in 35% of the curves, mainly in IVS and RLV. This is comparable to human medicine, where postsystolic motion is recorded in approximately 30% of myocardial segments in healthy humans.16

Most peak values had moderate to high variability, whereas time measurements had low variability. This might be attributed to measurement error during offline analysis. Sample area positioning has little impact on timings but substantially influences peak values because of the myocardial velocity gradient from the endocardium to epicardium. However, this is refuted by the fact that measurement variability of peak values was often low, whereas between-day intraobserver and within-day interobserver acquisition variability was moderate to high. This possibly reflects biological variability due to temporary changes of inotropic state or variation during image acquisition such as a different insonation angle. Similar results were found in previous studies3,17 of healthy dogs and cats; however, variability was lower in the present study, compared with previous studies6,7 of horses. This might be caused by the higher frame rate (> 180 frames/s).

The use of TDI in veterinary cardiology is a relatively recent development. Tissue Doppler imaging is more sensitive than conventional echocardiography for detection of systolic and diastolic myocardial dysfunction in cats with hypertrophic cardiomyopathy.4,18 Dogs with occult dilated cardiomyopathy have impaired LV relaxation as measured by TDI but not by conventional measurements.5 Tissue Doppler imaging can also detect diastolic dysfunction in dogs with chronic mitral valve regurgitation and decompensated congestive heart failure.19 This is correlated with left atrial dilatation and might be clinically applied to detect left atrial volume overload. In contrast, another study20 described few changes of TDI measurements in dogs with mitral valve regurgitation. The significantly different TDI measurements were covariate with changes of conventional parameters. Few studies are available on the use of TDI in larger groups of horses with cardiac disease. In 15 horses with atrial fibrillation, systolic and early diastolic velocities were significantly higher, whereas the late diastolic wave was absent.21 Tissue Doppler imaging has also been applied for follow-up of recovery of left atrial function after cardioversion of atrial fibrillation.22 A future application of TDI might be the early detection of myo-cardial dysfunction in horses with valvular disease.

The main limitations of this study were those inherent to the Doppler technique. Velocities are measured relative to the transducer, in the direction of the ultrasonographic beam. Velocity measurements are therefore affected by total heart motion and by the insonation angle between the ultrasonographic beam and wall motion. An adequate velocity scale is also a prerequisite. The Nyqvist limit of velocity measurement is based on the pulse repetition frequency in relation to the observed velocity. Exceeding this limit results in aliasing velocities, visible as a fast shift of high negative to high positive velocities or vice versa. Homogeneous myocardial coloring during acquisition indicates the absence of aliasing or artifacts.

Another limitation was that the results may only be valid for 2-D speckle tracking analyses by use of the same ultrasonographic machine, transducer, and offline analysis software and settings. Different settings might result in different variability of certain measurements. The results were not compared with a gold-standard technique because this is not available in horses. However, TDI has been extensively validated in vitro, in animal models, and in humans by comparison with tagged MRI and sonomicrometry.23–25 The present study included a small study population. A larger group would have allowed establishment of more accurate reference values and identification of influences of body weight, breed, heart rate, and training.

Results indicated that TDI measurements of radial velocity, strain rate, and strain were feasible in LV segments from right and left parasternal short-axis images at the papillary muscle and chordal levels. Tissue Doppler imaging allowed accurate timing of cardiac events, which was correlated to M-mode and pulsed-wave Doppler measurements. All timing measurements and several peak amplitudes had good repeatability and can be used in further clinical studies.

ABBREVIATIONS

A

Late diastolic peak measured by TDI, following the ECG P wave

CV

Coefficient of variation

E

Early diastolic peak measured by TDI, following the ECG R wave

EET

End ejection time measured in the TDI velocity and strain rate curves

IVC

Isovolumic contraction peak measured by TDI, following the ECG R wave

IVR

Isovolumic relaxation peak measured by TDI, following the ECG R wave

IVS

Interventricular septum

LLV

Left region of left ventricular free wall

LV

Left ventricular

LVFW

Left ventricular free wall

PEP

Pre-ejection period measured in the TDI velocity and strain rate curves

RLV

Right region of left ventricular free wall

St max

Maximal peak strain measured by TDI

St syst

Systolic peak strain measured by TDI

Syst

Systolic peak measured by TDI, following the ECG R wave

t

Time to peak measured from the preceding R or P wave

TDI

Tissue Doppler imaging

a.

GE Vivid 7 Dimension, GE Healthcare, Horten, Norway.

b.

3S Phased Array Transducer, GE Healthcare, Horten, Norway.

c.

EchoPAC Software, version 108.1.5, GE Healthcare, Horten, Norway.

d.

SPSS Statistics, version 17.0, release 17.0.1, SPSS Inc, Chicago, Ill.

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Contributor Notes

Supported by the Research Foundation Flanders (FWO-Vlaanderen).

Address correspondence to Dr. Decloedt (annelies.decloedt@ugent.be).