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Influence of heart rate on myocardial function using two-dimensional speckle-tracking echocardiography in healthy dogs
Journal of Veterinary Cardiology (2013) 15, 139e146
www.elsevier.com/locate/jvc
Influence of heart rate on myocardial function using two-dimensional speckle-tracking echocardiography in healthy dogs Ryohei Suzuki, DVM*, Hirotaka Matsumoto, DVM, PhD , Takahiro Teshima, DVM, PhD , Hidekazu Koyama, DVM, PhD Division of Veterinary Internal Medicine, Department of Veterinary Science, Faculty of Veterinary Medicine, Nippon Veterinary and Life Science University, 1-7-1 Kyonan-cho, Musashino-shi, Tokyo 1808602, Japan Received 9 May 2012; received in revised form 13 December 2012; accepted 13 December 2012
KEYWORDS Canine; Myocardial performance; Strain; Torsion; Ultrasound
Abstract Objective: The objective of this study was to evaluate the influence of heart rate (HR) on myocardial function assessed by two-dimensional speckle-tracking echocardiography (2D-STE) in healthy dogs. Animals: Thirteen healthy beagle dogs. Methods: Animals were anesthetized and HR was controlled with right atrial pacing. Myocardial function of each dog was assessed using 2D-STE at pacing rates of 120, 140, 160, and 180 bpm. Results: All strain and strain rate variables in the longitudinal, circumferential, and radial directions were not significantly different between pacing rates. Peak early diastolic torsion rate at 180 bpm was significantly increased compared with that at 120 bpm (P ¼ 0.003). Conclusion: Torsion rate in early diastole was elevated at 180 bpm, which may reflect improved myocardial relaxation with higher HR. Changes in left ventricular torsion during tachycardia may play an important role in preserving stroke volume in the presence of shortened ejection and filling times. ª 2013 Elsevier B.V. All rights reserved.
* Corresponding author. E-mail address: [email protected] (R. Suzuki). 1760-2734/$ - see front matter ª 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.jvc.2012.12.004
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Abbreviations 2D Em HR LV STE SV
two-dimensional early diastolic mitral annular velocity derived by pulsed Doppler technique heart rate left ventricular speckle-tracking echocardiography stroke volume
Introduction Echocardiography plays an essential role in the assessment of cardiac disease in veterinary medicine. Two-dimensional speckle-tracking echocardiography (2D-STE) has recently been used to assess myocardial deformations in humans1e3 and dogs.4e8 This technique has enabled the assessment of myocardial variables, such as strain, strain rate, and torsional measurements, that provide better quantification of regional and global myocardial deformations1e8 and might have higher sensitivity than conventional echocardiographic parameters for detecting subtle myocardial function abnormalities.2,9,10 The tissue Doppler technique is often used to evaluate myocardial function, but the measurements using this technique are affected by translational motion of the heart, tethering of surrounding myocardium, and Doppler angle.11 The 2D-STE method tracks grayscale B-mode images of unique speckle patterns in the myocardium; therefore, its findings should be relatively independent of cardiac translation, tethering, and angle.1 Furthermore, 2D-STE enables the assessment of myocardial function in 3 directions (longitudinal, circumferential, radial) and one motionoriented original myofiber orientation (torsional motion).3,5,8 However, this multidirectional assessment of myocardial function by 2D-STE in the same dogs, even healthy dogs, has not previously been reported. Heart rate (HR) is a known important modulator of cardiac function, influencing echocardiographic variables.12,13 Therefore, it should always be considered in the evaluation of cardiac function, particularly in the event of heart failure.14 However, influence of HR on myocardial function assessed by 2D-STE has not previously been reported. Therefore, the purpose of our study was to evaluate the influence of HR on myocardial function assessed by 2D-STE in healthy anesthetized dogs. We hypothesized that elevation of HR would
increase left ventricular (LV) systolic and diastolic function and that 2D-STE would be diagnostically useful in the multidirectional quantification of these changes in healthy anesthetized dogs.
Animals, materials and methods Animals Thirteen healthy beagles (body weight, 10.6 2.0 kg; age, 12.0 0.5 months) were used in this study. All dogs were confirmed to be healthy based on no history of cardiac signs as well as normal findings on a complete physical examination, complete blood count, serum biochemistry evaluation, ECG, thoracic radiography, and transthoracic echocardiography.
Anesthesia All dogs were administered intravenous thiopental sodium at a dose of 25 mg/kg for induction of anesthesia, maintained with 1e1.5% isoflurane mixed with 100% oxygen, and manually ventilated with a tidal volume of 15e20 mL/kg at a rate of 10e15 per minute.
Pacing protocol Each dog was placed in left lateral recumbency for instrumentation. The right lateral neck region was clipped, prepared aseptically, and draped. An approximately 5-cm surgical cutdown was performed over the right jugular furrow to expose the right jugular vein. An electrophysiology cathetera was directly inserted into the right jugular vein under echocardiographic and fluoroscopic guidance and fixed within the right atrial cavity for controlled right atrial pacing via an external programmable pacemaker.b The catheter position was adjusted to obtain stable atrial pacing data, as needed. All dogs were examined after 5 min of continuous atrial pacing at rates of 120, 140, 160, and 180 bpm using the same order of pacing rates in all dogs. Echocardiographic data and a single limb lead ECG were simultaneously recorded and stored digitally during continuous pacing at each HR state. At least 5-min intervals were allowed for hemodynamic stabilization between each pacing period. After the conclusion of the experiment about 1.5 h after induction of anesthesia, the a b
5F electrophysiology catheter, St. Jude Medical, MN, USA. Model SEP-101; Star Medical Inc., Tokyo, Japan.
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catheter was removed and the jugular vein was ligated. Standard surgical closure of the incision was performed, and the dogs were closely observed until they were extubated and had completely recovered from anesthesia. All dogs were then transferred to another protocol within our institution. Procedures were performed according to the Guide for Care and Use of Laboratory Animals and approved by the ethical committee for laboratory animal use of Nippon Veterinary and Life Science University, Japan.
apical 5-chamber view. Peak velocity and ejection time of the LV outflow were measured. Stroke volume (SV) was estimated from the product of aortic valve cross-area and aortic outflow time-velocity integral.20 The cross-sectional area of the aortic annulus was calculated as p r2, where r represents 1/2 of the annulus diameter. The aortic valve annulus diameter was obtained from the right parasternal long-axis view with the zoom option using the inner edge to inner edge method.20 The mean value of 3 consecutive cardiac cycles for each measurement was used in the analysis.
Standard echocardiography Conventional 2D, M-mode, and Doppler examinations were performed during each pacing period by a single trained investigator (H.K.) using a Vivid7 echocardiographic systemc and a 3.5e6.9 MHz transducer. A simultaneous ECG limb lead II was recorded and displayed on the images. All data were obtained from at least 5 consecutive cardiac cycles in stable pacing rhythm and at end expiration from dogs that were positioned on a table designed to allow echocardiographic examinations during cardiac catheterization. The surgical region of all dogs was draped and packed with antiseptic dressing and the dogs were carefully and repeatedly repositioned in the right and left lateral recumbent position. Only echocardiographic recordings from beats during 1:1 atrioventricular conduction were examined. Images were analyzed using an offline EchoPAC workstation3 by a single observer. The left atrial-to-aortic root ratio was obtained from the right parasternal short-axis view using the B-mode method.15 M-mode measurements of the LV were obtained from the right parasternal short-axis view at the level of the chordae tendineae using the leading edge-to-leading edge method.16 These measurements included end-diastolic LV internal dimension, end-systolic LV internal dimension, and fractional shortening. Transmitral flow was obtained from the left apical 4-chamber view, and the peak velocity of the early diastolic wave (E wave), deceleration time of the E wave, and peak velocity of the late diastolic wave (A wave) were measured.17,18 Whenever E and A waves were fused, the E and A wave and the E wave deceleration time values were not analyzed. Mitral annular motion velocity derived via pulsed wave Doppler technique was obtained from the interventricular septum from the left apical 4-chamber view. Peak velocity of early diastolic mitral annular motion (Em) was measured.18,19 Aortic outflow signals were acquired by pulsed wave Doppler and obtained from a left c
GE Healthcare, Tokyo, Japan.
2D-STE After the standard conventional 2D, M-mode, and Doppler examinations were completed, highquality images for 2D-STE analysis were carefully obtained by the same investigator using the same echocardiographic system and transducer as described for standard echocardiography. For analysis of the 2D-STE data, all views were recorded at rates of 70e156 frames per second; specifically, frame rate was increased with increasing HR. To evaluate radial and circumferential deformations by 2D-STE, we used a right parasternal short-axis view of the LV at the level of the papillary muscles. We used a left apical 4-chamber view for analysis of longitudinal deformations. For torsional deformations, we used a right parasternal short-axis view of the LV with recordings made at both the basal and apical imaging planes. Proper basal and apical short-axis views were carefully obtained using the following anatomic landmarks: at the basal level, the mitral valve and at the apical level, the LV cavity alone with no visible papillary muscles. All data were obtained for at least 5 consecutive cardiac cycles during stable pacing rhythm. Images were analyzed by a single observer using an offline EchoPAC workstation as described previously.7,8 We selected one cardiac cycle (from one QRS complex to the next QRS complex) from the high-quality images and manually traced the endocardial borders of the myocardium at end-diastole to select the appropriate region of interest. The region of interest was then adjusted to incorporate the entire myocardial thickness and checked by the observer to ensure that it was visually synchronized with the cardiac movement throughout the entire cardiac cycle. The computer software automatically traced the myocardium, created 6 segments in each image, and evaluated whether it reliably followed myocardial motions. If the initial evaluation failed because the region of interest could not be traced during myocardial movement, we
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Table 1 Conventional 2D, M-mode, and Doppler data (mean SD) at different pacing rates from 13 healthy anesthetized beagle dogs. Variable
HR (bpm) 120
Left atrial to aortic root ratio End diastolic LV internal dimension (mm) End systolic LV internal dimension (mm) Fractional shortening (%) E wave velocity (m/s) E wave deceleration time (ms) A wave velocity (m/s) Em velocity (cm/s) LV outflow velocity (m/s) LV ejection time (ms) Stroke volume (mL)
1.4 25.3 19.4 23.2 0.65 112 0.39 6.0 0.9 205.5 19.0
140 0.1 3.0 2.9 5.9 0.11 15 0.11 1.1 0.2 15.7 2.5
1.3 25.2 20.1 20.5 0.69 108 0.43 6.5 0.9 190.5 16.8
160 0.1 3.4 3.4 5.6 0.12 19 0.18 1.8 0.2 15.0 3.5
1.4 24.3 19.2 20.7 0.79 84 0.50 7.3 0.9 175.5 16.7
0.1 3.4 3.0 8.8 0.14 15a,b 0.19 1.3 0.2 11.3a 5.1
180 1.4 23.7 18.8 19.9 0.85 84 0.51 8.7 0.9 163.9 17.6
0.1 3.3 2.1 7.3 0.19a 11a,b 0.14 1.8a,b 0.1 13.9a,b 5.0
HR, heart rate; LV, left ventricular; E wave, early diastolic transmitral wave; A wave, late diastolic transmitral wave; Em, early diastolic mitral annular motion derived using the tissue Doppler technique. a Within a row, the value differs significantly (P < 0.008) from the value at 120 bpm. b Within a row, the value differs significantly (P < 0.008) from the value at 140 bpm.
retraced the endocardial borders and manually corrected them, as needed. If multiple evaluation attempts failed, the failed segment was excluded from the analysis. Finally, we measured the peak strain and strain rate during systole and early diastole in the longitudinal, circumferential, and radial directions. We used the mean of all 6 segmental values for all variables. Peak systolic and early diastolic values were defined as the maximal deflections of the respective curves during the ejection and early diastolic phases as identified from the ECG. We stored each frame values in each basal and apical view and then obtained peak systolic and early diastolic values of rotation and the rotation rate of each view. We then calculated torsion and torsion rate as a net difference of the values of each frame between the basal and apical segments as previously reported in humans3 and dogs.5,8 Counterclockwise rotation/torsion viewed from the apex was expressed as a positive value. The mean values of the measurements from 3 consecutive cardiac cycles from high-quality images were used in all analyses.
Statistical analysis Data are expressed as mean SD. All statistical analyses were performed using a commercially available computer software.d The KolmogoroveSmirnov test was used to check the normal distribution of the variables. We used repeated measures analysis of variances (ANOVA) to test the d
SPSS version 15.0J for Windows; SPSS, Tokyo, Japan.
equality of the means among the 4 different pacing methods. Variables that demonstrated significant differences among groups by the ANOVA test were then compared using Tukey’s honestly significant difference test with Bonferroni’s adjustment. Values of P 0.008 were considered significant. Intraobserver measurement variability for 2D-STE was assessed using the coefficient of variation from 5 dogs paced at 120 bpm selected at random by repeating the measurements on different days. The coefficient of variation was determined as the ratio of the standard deviation to the mean values.
Results Standard echocardiography Two dogs were excluded from the analysis at an HR of 120 bpm because of competition between paced and inherent beats. Results of 2D, M-mode, and Doppler examinations at different HRs are shown in Table 1. Peak E wave velocity at 180 bpm was significantly increased compared with that at 120 bpm (P ¼ 0.008). Em velocity at 180 bpm was significantly increased compared with that at 120 and 140 bpm (P ¼ 0.001 and P ¼ 0.006, respectively). E wave deceleration time was significantly shortened at 160 and 180 bpm compared with that at 120 and 140 bpm (160 bpm: P < 0.001 and P ¼ 0.002; 180 bpm: P < 0.001 and P ¼ 0.002, respectively). LV ejection time was significantly shortened at 180 bpm compared with that at 120 and 140 bpm (P < 0.001 and P < 0.001, respectively). LV ejection time was also
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Table 2 Systolic and early diastolic myocardial strain and strain rate variables (mean SD) using twodimensional speckle-tracking echocardiography at different pacing rates in 13 healthy anesthetized beagle dogs. Variable
HR (bpm) 120
Systolic long S (%) Systolic long Sr (1/s) Early diastolic long Sr (1/s) Systolic rad S (%) Systolic rad Sr (1/s) Early diastolic rad Sr (1/s) Systolic circ S (%) Systolic circ Sr (1/s) Early diastolic circ Sr (1/s)
11.3 1.1 1.4 44.6 2.4 2.9 12.0 1.4 1.1
140 9.9 1.1 1.0 40.7 2.3 2.5 10.5 1.3 1.0
3.1 0.3 0.4 10.6 0.5 0.8 2.2 0.3 0.4
160 10.2 1.2 0.6 38.4 2.6 1.8 9.4 1.3 0.9
2.7 0.3 0.6 11.8 0.6 1.0 2.4 0.3 0.5
180 3.1 0.3 0.5 10.0 0.9 1.2 2.7 0.3 0.5
8.9 1.2 0.8 33.2 2.6 2.5 8.4 1.4 1.1
2.8 0.4 0.8 7.9 0.4 1.6 2.3 0.3 0.4
Long S, longitudinal strain; Long Sr, longitudinal strain rate; Rad S, radial strain; Rad Sr, radial strain rate; Circ S, circumferential strain; Circ Sr, circumferential strain rate.
significantly shortened at 160 bpm compared with that at 120 bpm (P < 0.001). In contrast, left atrial dimension, LV internal dimension in systole and diastole, and SV were not significantly different at different HRs.
shown in Table 3. The peak early diastolic torsion rate at 180 bpm was significantly increased compared with that at 120 bpm (P ¼ 0.003). Plots of individual dogs’ peak early diastolic torsion rate are shown in Figure 1. Other deformation parameters in diastole were not significantly different.
2D-STE All myocardial segments for short-axis and long-axis speckle tracking images were included in the statistical analysis. The coefficient of variation (minimumemaximum) of intraobserver 2D-STE measurements were 0.2e13.5% for radial deformations, 0.2e10.1% for circumferential deformations, 0.1e17.1% for longitudinal deformations, and 0.7e16.6% for torsional motions. The results of systolic and diastolic myocardial strain and strain rate variables using 2D-STE at different HRs are shown in Table 2. All strain and strain rate variables were not significantly different at the range of 120e180 bpm. The results of systolic and diastolic myocardial torsional variables using 2D-STE at different HRs are
Discussion Multidirectional myocardial deformations could be assessed using 2D-STE to evaluate myocardial function at HRs of 120e180 bpm in healthy anesthetized beagles. Strain and strain rate variables were not changed by increases in HR. However, the torsion rate in early diastole was elevated at an HR of 180 bpm. In this study, strain and strain rate variables in the longitudinal, circumferential, and radial directions were not changed with increasing HR for reasons incompletely understood. Possibly, LV performance assessed using strain and strain rate
Table 3 Systolic and early diastolic myocardial torsional variables (mean SD) using two-dimensional speckletracking echocardiography at different pacing rates in 13 healthy anesthetized beagle dogs. Variable
HR (bpm) 120
Systolic basal rotation ( ) Systolic basal rotation rate ( /s) Early diastolic basal rotation rate ( /s) Systolic apical rotation ( ) Systolic apical rotation rate ( /s) Early diastolic apical rotation rate ( /s) Systolic torsion ( ) Systolic torsion rate ( /s) Early diastolic torsion rate ( /s) a
2.9 66.8 42.0 9.3 110.8 87.6 8.6 95.5 96.1
140 1.6 31.6 26.7 3.8 44.3 36.1 3.8 40.6 36.0
3.4 75.3 51.5 9.7 121.5 107.4 10.2 106.8 108.2
160 1.9 22.2 36.7 3.2 41.5 27.7 3.1 45.3 43.6
Within a row, the value differs significantly (P < 0.008) from the value at 120 bpm.
4.2 77.1 43.5 8.2 106.6 86.0 10.0 124.7 110.2
180 2.4 24.5 41.3 3.7 50.4 36.5 4.5 58.3 36.4
4.1 83.7 75.9 8.5 124.5 118.0 11.0 136.9 161.9
2.2 23.5 45.6 2.7 56.5 44.7 3.0 40.9 51.3a
144 variables did not change to a sufficiently substantial degree to be detected. These findings are in agreement with those of an earlier study.21 In contrast, the torsion rate in early diastole was elevated at an HR of 180 bpm. LV torsion is reported to reflect the balance of function between the subendomyocardium and subepimyocardium.22 The greater torsional deformation in early diastole observed at higher HR may be caused by a decrease in the myocardial function of the subendomyocardium and an increase in subepimyocardial function in the presence of shortened ejection and filling times. With increasing HR, diastole is reduced more than systole. Because coronary blood flow to the endomyocardium mainly occurs in diastole,23 subendomyocardial function may be affected more compared to that of the subepimyocardium with increasing HRs. Furthermore, because both the subepimyocardium and subendomyocardium work together to produce a nearly homogenous transmural distribution of myocardial stress and fiber strain during ejection,24 a decrease in subendomyocardial function may be compensated by an increase in subepimyocardial function. Therefore, decreased myocardial function in the subendomyocardium combined with a compensatory increase in subepimyocardial function could be the cause for the greater torsional deformation observed at an HR of 180 bpm. The left ventricle isovolumic contraction and relaxation times decrease with increasing HR. Moreover, diastole, and thus the relaxation component, is more influenced by increasing HR than systole. Isovolumic contraction is a dynamic process characterized by layer-dependent deformations.25 The dynamic interaction between subendomyocardial and subepimyocardial fiber helices in the LV according to each layer-
R. Suzuki et al. dependent contraction leads to a twisting motion.26 Furthermore, the potential energy stored in the twisted LV is rapidly released in early diastole, leading to swift recoil of the LV during isovolumic relaxation.22 The details of myocardial function in this phase of the cardiac cycle have not been assessed non-invasively using conventional echocardiography. In this study, the torsion rate in early diastole was elevated at an HR of 180 bpm. In accordance with the findings of earlier studies27e29 and based on the fact that LV torsion is determined by the orientation of the helical myocardial fibers,30,31 the early diastolic torsion rate might reflect enhanced myocardial relaxation and may provide additional non-invasive insight into LV diastolic function, particularly during the isovolumic period. LV torsion is thought to be a mechanism by which the ventricle equalizes transmural oxygen demand gradients, thus minimizing oxygen consumption and optimizing myocardial energetics and efficiency.32e34 The increase in the diastolic torsion rate associated with high HR suggests an improvement of the LV ability to modulate transmural metabolic gradients, which might result in SV maintenance against shortened ejection and filling times. Our study has several limitations. The small number of dogs may affect the statistical power and limit extrapolation of our findings to larger populations. Because of the study design, the effects of anesthesia on myocardial function could not be eliminated. Therefore, our findings should not be extrapolated to conscious dogs. Calculation of LV torsion depends on non-simultaneous measurements of two segments (base and apex), which may have affected our results. In addition, myocardial rotation is reported to be dependent on transducer angulation35 and the true apex of the left ventricle needed for 2D-STE analysis might not be technically acquirable. Speckle imaging as determined by three-dimensional echocardiography in a future study may resolve these limitations. Only normal dogs were examined, however myocardial function assessed by 2D-STE may vary between normal and failing remodeled hearts. Finally, future work incorporating pressure-volume loop analysis for a more accurate evaluation of cardiac function is warranted.
Conclusions Figure 1 Plots of individual dogs’ peak early diastolic LV torsion rate assessed by two-dimensional speckletracking echocardiography at the pacing rates of 120, 140, 160, and 180 bpm.
Myocardial deformations were assessed using 2DSTE at HRs between 120 and 180 bpm in healthy anesthetized beagles. Torsion rate in early diastole
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145
was elevated only at 180 bpm HR, which may reflect increased myocardial relaxation with increasing HR. Enhanced LV torsion at higher HR may play an important role in preserving SV in the presence of shortened ejection and filling times. Although further studies are needed, 2D-STE examinations of myocardial deformations might provide important noninvasive information on myocardial contractile function.
deformation, but depressed longitudinal and radial deformation in patients with diastolic heart failure. Eur Heart J 2008;29:1283e1289. Mizuguchi Y, Oishi Y, Miyoshi H, Iuchi A, Nagase N, Oki T. The functional role of longitudinal, circumferential, and radial myocardial deformation for regulating the early impairment of left ventricular contraction and relaxation in patients with cardiovascular risk factors: a study with twodimensional strain imaging. J Am Soc Echocardiogr 2008; 21:1138e1144. Lim P, Mitchell-Heggs L, Buakhamsri A, Thomas JD, Grimm RA. Impact of left ventricular size on tissue Doppler and longitudinal strain by speckle tracking for assessing wall motion and mechanical dyssynchrony in candidates for cardiac resynchronization therapy. J Am Soc Echocardiogr 2009;22:695e701. Jacobs G, Mahjoob K. Influence of alterations in heart rate on echocardiographic measurements in the dog. Am J Vet Res 1988;49:548e552. Yamamoto K, Masuyama T, Tanouchi J, Doi Y, Kondo H, Hori M, Kitabatake A, Kamada T. Effects of heart rate on left ventricular filling dynamics: assessment from simultaneous recordings of pulsed Doppler transmitral flow velocity pattern and haemodynamic variables. Cardiovasc Res 1993; 27:935e941. Crosara S, Borgarelli M, Perego M, Ha ¨ggstro ¨m J, La Rosa G, Tarducci A, Santilli RA. Holter monitoring in 36 dogs with myxomatous mitral valve disease. Aust Vet J 2010;88: 386e392. Rishniw M, Erb HN. Evaluation of four 2-dimensional echocardiographic methods of assessing left atrial size in dogs. J Vet Intern Med 2000;14:429e435. Sahn DJ, DeMaria A, Kisslo J, Weyman A. Recommendations regarding quantitation in M-mode echocardiography: results of a survey of echocardiographic measurements. Circulation 1978;58:1072e1083. Schober KE, Hart TM, Stern JA, Li X, Samii VF, Zekas LJ, Scansen BA, Bonagura JD. Detection of congestive heart failure in dogs by Doppler echocardiography. J Vet Intern Med 2010;24:1358e1368. Nagueh SF, Appleton CP, Gillebert TC, Marino PN, Oh JK, Smiseth OA, Waggoner AD, Flachskampf FA, Pellikka PA, Evangelista A. Recommendations for the evaluation of left ventricular diastolic function by echocardiography. J Am Soc Echocardiogr 2009;22:107e133. Teshima K, Asano K, Sasaki Y, Kato Y, Kutara K, Edamura K, Hasegawa A, Tanaka S. Assessment of left ventricular function using pulsed tissue Doppler imaging in healthy dogs and dogs with spontaneous mitral regurgitation. J Vet Med Sci 2005;67:1207e1215. Lewis JF, Kuo LC, Nelson JG, Limacher MC, Quinones MA. Pulsed Doppler echocardiographic determination of stroke volume and cardiac output: clinical validation of two new methods using the apical window. Circulation 1984;70: 425e431. Weidemann F, Jamal F, Sutherland GR, Claus P, Kowalski M, Hatle L, De Scheerder I, Bijnens B, Rademakers FE. Myocardial function defined by strain rate and strain during alterations in inotropic states and heart rate. Am J Physiol Heart Circ Physiol 2002;283:H792eH799. Takeuchi M, Otsuji Y, Lang RM. Evaluation of left ventricular function using left ventricular twist and torsion parameters. Curr Cardiol Rep 2009;11:225e230. Domalik-Wawrzynski LJ, Powell Jr WJ, Guerrero L, Palacios I. Effect of changes in ventricular relaxation on early diastolic coronary blood flow in canine hearts. Circ Res 1987;61:747e756.
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Conflicts of interest None.
Acknowledgments
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The authors wish to thank Syo Miyazawa and Tetsuya Uematsu for their technical assistance. 14.
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Influence of heart rate on myocardial function using two-dimensional speckle-tracking echocardiography in healthy dogs Ryohei Suzuki, DVM*, Hirotaka Matsumoto, DVM, PhD , Takahiro Teshima, DVM, PhD , Hidekazu Koyama, DVM, PhD Division of Veterinary Internal Medicine, Department of Veterinary Science, Faculty of Veterinary Medicine, Nippon Veterinary and Life Science University, 1-7-1 Kyonan-cho, Musashino-shi, Tokyo 1808602, Japan Received 9 May 2012; received in revised form 13 December 2012; accepted 13 December 2012
KEYWORDS Canine; Myocardial performance; Strain; Torsion; Ultrasound
Abstract Objective: The objective of this study was to evaluate the influence of heart rate (HR) on myocardial function assessed by two-dimensional speckle-tracking echocardiography (2D-STE) in healthy dogs. Animals: Thirteen healthy beagle dogs. Methods: Animals were anesthetized and HR was controlled with right atrial pacing. Myocardial function of each dog was assessed using 2D-STE at pacing rates of 120, 140, 160, and 180 bpm. Results: All strain and strain rate variables in the longitudinal, circumferential, and radial directions were not significantly different between pacing rates. Peak early diastolic torsion rate at 180 bpm was significantly increased compared with that at 120 bpm (P ¼ 0.003). Conclusion: Torsion rate in early diastole was elevated at 180 bpm, which may reflect improved myocardial relaxation with higher HR. Changes in left ventricular torsion during tachycardia may play an important role in preserving stroke volume in the presence of shortened ejection and filling times. ª 2013 Elsevier B.V. All rights reserved.
* Corresponding author. E-mail address: [email protected] (R. Suzuki). 1760-2734/$ - see front matter ª 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.jvc.2012.12.004
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Abbreviations 2D Em HR LV STE SV
two-dimensional early diastolic mitral annular velocity derived by pulsed Doppler technique heart rate left ventricular speckle-tracking echocardiography stroke volume
Introduction Echocardiography plays an essential role in the assessment of cardiac disease in veterinary medicine. Two-dimensional speckle-tracking echocardiography (2D-STE) has recently been used to assess myocardial deformations in humans1e3 and dogs.4e8 This technique has enabled the assessment of myocardial variables, such as strain, strain rate, and torsional measurements, that provide better quantification of regional and global myocardial deformations1e8 and might have higher sensitivity than conventional echocardiographic parameters for detecting subtle myocardial function abnormalities.2,9,10 The tissue Doppler technique is often used to evaluate myocardial function, but the measurements using this technique are affected by translational motion of the heart, tethering of surrounding myocardium, and Doppler angle.11 The 2D-STE method tracks grayscale B-mode images of unique speckle patterns in the myocardium; therefore, its findings should be relatively independent of cardiac translation, tethering, and angle.1 Furthermore, 2D-STE enables the assessment of myocardial function in 3 directions (longitudinal, circumferential, radial) and one motionoriented original myofiber orientation (torsional motion).3,5,8 However, this multidirectional assessment of myocardial function by 2D-STE in the same dogs, even healthy dogs, has not previously been reported. Heart rate (HR) is a known important modulator of cardiac function, influencing echocardiographic variables.12,13 Therefore, it should always be considered in the evaluation of cardiac function, particularly in the event of heart failure.14 However, influence of HR on myocardial function assessed by 2D-STE has not previously been reported. Therefore, the purpose of our study was to evaluate the influence of HR on myocardial function assessed by 2D-STE in healthy anesthetized dogs. We hypothesized that elevation of HR would
increase left ventricular (LV) systolic and diastolic function and that 2D-STE would be diagnostically useful in the multidirectional quantification of these changes in healthy anesthetized dogs.
Animals, materials and methods Animals Thirteen healthy beagles (body weight, 10.6 2.0 kg; age, 12.0 0.5 months) were used in this study. All dogs were confirmed to be healthy based on no history of cardiac signs as well as normal findings on a complete physical examination, complete blood count, serum biochemistry evaluation, ECG, thoracic radiography, and transthoracic echocardiography.
Anesthesia All dogs were administered intravenous thiopental sodium at a dose of 25 mg/kg for induction of anesthesia, maintained with 1e1.5% isoflurane mixed with 100% oxygen, and manually ventilated with a tidal volume of 15e20 mL/kg at a rate of 10e15 per minute.
Pacing protocol Each dog was placed in left lateral recumbency for instrumentation. The right lateral neck region was clipped, prepared aseptically, and draped. An approximately 5-cm surgical cutdown was performed over the right jugular furrow to expose the right jugular vein. An electrophysiology cathetera was directly inserted into the right jugular vein under echocardiographic and fluoroscopic guidance and fixed within the right atrial cavity for controlled right atrial pacing via an external programmable pacemaker.b The catheter position was adjusted to obtain stable atrial pacing data, as needed. All dogs were examined after 5 min of continuous atrial pacing at rates of 120, 140, 160, and 180 bpm using the same order of pacing rates in all dogs. Echocardiographic data and a single limb lead ECG were simultaneously recorded and stored digitally during continuous pacing at each HR state. At least 5-min intervals were allowed for hemodynamic stabilization between each pacing period. After the conclusion of the experiment about 1.5 h after induction of anesthesia, the a b
5F electrophysiology catheter, St. Jude Medical, MN, USA. Model SEP-101; Star Medical Inc., Tokyo, Japan.
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catheter was removed and the jugular vein was ligated. Standard surgical closure of the incision was performed, and the dogs were closely observed until they were extubated and had completely recovered from anesthesia. All dogs were then transferred to another protocol within our institution. Procedures were performed according to the Guide for Care and Use of Laboratory Animals and approved by the ethical committee for laboratory animal use of Nippon Veterinary and Life Science University, Japan.
apical 5-chamber view. Peak velocity and ejection time of the LV outflow were measured. Stroke volume (SV) was estimated from the product of aortic valve cross-area and aortic outflow time-velocity integral.20 The cross-sectional area of the aortic annulus was calculated as p r2, where r represents 1/2 of the annulus diameter. The aortic valve annulus diameter was obtained from the right parasternal long-axis view with the zoom option using the inner edge to inner edge method.20 The mean value of 3 consecutive cardiac cycles for each measurement was used in the analysis.
Standard echocardiography Conventional 2D, M-mode, and Doppler examinations were performed during each pacing period by a single trained investigator (H.K.) using a Vivid7 echocardiographic systemc and a 3.5e6.9 MHz transducer. A simultaneous ECG limb lead II was recorded and displayed on the images. All data were obtained from at least 5 consecutive cardiac cycles in stable pacing rhythm and at end expiration from dogs that were positioned on a table designed to allow echocardiographic examinations during cardiac catheterization. The surgical region of all dogs was draped and packed with antiseptic dressing and the dogs were carefully and repeatedly repositioned in the right and left lateral recumbent position. Only echocardiographic recordings from beats during 1:1 atrioventricular conduction were examined. Images were analyzed using an offline EchoPAC workstation3 by a single observer. The left atrial-to-aortic root ratio was obtained from the right parasternal short-axis view using the B-mode method.15 M-mode measurements of the LV were obtained from the right parasternal short-axis view at the level of the chordae tendineae using the leading edge-to-leading edge method.16 These measurements included end-diastolic LV internal dimension, end-systolic LV internal dimension, and fractional shortening. Transmitral flow was obtained from the left apical 4-chamber view, and the peak velocity of the early diastolic wave (E wave), deceleration time of the E wave, and peak velocity of the late diastolic wave (A wave) were measured.17,18 Whenever E and A waves were fused, the E and A wave and the E wave deceleration time values were not analyzed. Mitral annular motion velocity derived via pulsed wave Doppler technique was obtained from the interventricular septum from the left apical 4-chamber view. Peak velocity of early diastolic mitral annular motion (Em) was measured.18,19 Aortic outflow signals were acquired by pulsed wave Doppler and obtained from a left c
GE Healthcare, Tokyo, Japan.
2D-STE After the standard conventional 2D, M-mode, and Doppler examinations were completed, highquality images for 2D-STE analysis were carefully obtained by the same investigator using the same echocardiographic system and transducer as described for standard echocardiography. For analysis of the 2D-STE data, all views were recorded at rates of 70e156 frames per second; specifically, frame rate was increased with increasing HR. To evaluate radial and circumferential deformations by 2D-STE, we used a right parasternal short-axis view of the LV at the level of the papillary muscles. We used a left apical 4-chamber view for analysis of longitudinal deformations. For torsional deformations, we used a right parasternal short-axis view of the LV with recordings made at both the basal and apical imaging planes. Proper basal and apical short-axis views were carefully obtained using the following anatomic landmarks: at the basal level, the mitral valve and at the apical level, the LV cavity alone with no visible papillary muscles. All data were obtained for at least 5 consecutive cardiac cycles during stable pacing rhythm. Images were analyzed by a single observer using an offline EchoPAC workstation as described previously.7,8 We selected one cardiac cycle (from one QRS complex to the next QRS complex) from the high-quality images and manually traced the endocardial borders of the myocardium at end-diastole to select the appropriate region of interest. The region of interest was then adjusted to incorporate the entire myocardial thickness and checked by the observer to ensure that it was visually synchronized with the cardiac movement throughout the entire cardiac cycle. The computer software automatically traced the myocardium, created 6 segments in each image, and evaluated whether it reliably followed myocardial motions. If the initial evaluation failed because the region of interest could not be traced during myocardial movement, we
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Table 1 Conventional 2D, M-mode, and Doppler data (mean SD) at different pacing rates from 13 healthy anesthetized beagle dogs. Variable
HR (bpm) 120
Left atrial to aortic root ratio End diastolic LV internal dimension (mm) End systolic LV internal dimension (mm) Fractional shortening (%) E wave velocity (m/s) E wave deceleration time (ms) A wave velocity (m/s) Em velocity (cm/s) LV outflow velocity (m/s) LV ejection time (ms) Stroke volume (mL)
1.4 25.3 19.4 23.2 0.65 112 0.39 6.0 0.9 205.5 19.0
140 0.1 3.0 2.9 5.9 0.11 15 0.11 1.1 0.2 15.7 2.5
1.3 25.2 20.1 20.5 0.69 108 0.43 6.5 0.9 190.5 16.8
160 0.1 3.4 3.4 5.6 0.12 19 0.18 1.8 0.2 15.0 3.5
1.4 24.3 19.2 20.7 0.79 84 0.50 7.3 0.9 175.5 16.7
0.1 3.4 3.0 8.8 0.14 15a,b 0.19 1.3 0.2 11.3a 5.1
180 1.4 23.7 18.8 19.9 0.85 84 0.51 8.7 0.9 163.9 17.6
0.1 3.3 2.1 7.3 0.19a 11a,b 0.14 1.8a,b 0.1 13.9a,b 5.0
HR, heart rate; LV, left ventricular; E wave, early diastolic transmitral wave; A wave, late diastolic transmitral wave; Em, early diastolic mitral annular motion derived using the tissue Doppler technique. a Within a row, the value differs significantly (P < 0.008) from the value at 120 bpm. b Within a row, the value differs significantly (P < 0.008) from the value at 140 bpm.
retraced the endocardial borders and manually corrected them, as needed. If multiple evaluation attempts failed, the failed segment was excluded from the analysis. Finally, we measured the peak strain and strain rate during systole and early diastole in the longitudinal, circumferential, and radial directions. We used the mean of all 6 segmental values for all variables. Peak systolic and early diastolic values were defined as the maximal deflections of the respective curves during the ejection and early diastolic phases as identified from the ECG. We stored each frame values in each basal and apical view and then obtained peak systolic and early diastolic values of rotation and the rotation rate of each view. We then calculated torsion and torsion rate as a net difference of the values of each frame between the basal and apical segments as previously reported in humans3 and dogs.5,8 Counterclockwise rotation/torsion viewed from the apex was expressed as a positive value. The mean values of the measurements from 3 consecutive cardiac cycles from high-quality images were used in all analyses.
Statistical analysis Data are expressed as mean SD. All statistical analyses were performed using a commercially available computer software.d The KolmogoroveSmirnov test was used to check the normal distribution of the variables. We used repeated measures analysis of variances (ANOVA) to test the d
SPSS version 15.0J for Windows; SPSS, Tokyo, Japan.
equality of the means among the 4 different pacing methods. Variables that demonstrated significant differences among groups by the ANOVA test were then compared using Tukey’s honestly significant difference test with Bonferroni’s adjustment. Values of P 0.008 were considered significant. Intraobserver measurement variability for 2D-STE was assessed using the coefficient of variation from 5 dogs paced at 120 bpm selected at random by repeating the measurements on different days. The coefficient of variation was determined as the ratio of the standard deviation to the mean values.
Results Standard echocardiography Two dogs were excluded from the analysis at an HR of 120 bpm because of competition between paced and inherent beats. Results of 2D, M-mode, and Doppler examinations at different HRs are shown in Table 1. Peak E wave velocity at 180 bpm was significantly increased compared with that at 120 bpm (P ¼ 0.008). Em velocity at 180 bpm was significantly increased compared with that at 120 and 140 bpm (P ¼ 0.001 and P ¼ 0.006, respectively). E wave deceleration time was significantly shortened at 160 and 180 bpm compared with that at 120 and 140 bpm (160 bpm: P < 0.001 and P ¼ 0.002; 180 bpm: P < 0.001 and P ¼ 0.002, respectively). LV ejection time was significantly shortened at 180 bpm compared with that at 120 and 140 bpm (P < 0.001 and P < 0.001, respectively). LV ejection time was also
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Table 2 Systolic and early diastolic myocardial strain and strain rate variables (mean SD) using twodimensional speckle-tracking echocardiography at different pacing rates in 13 healthy anesthetized beagle dogs. Variable
HR (bpm) 120
Systolic long S (%) Systolic long Sr (1/s) Early diastolic long Sr (1/s) Systolic rad S (%) Systolic rad Sr (1/s) Early diastolic rad Sr (1/s) Systolic circ S (%) Systolic circ Sr (1/s) Early diastolic circ Sr (1/s)
11.3 1.1 1.4 44.6 2.4 2.9 12.0 1.4 1.1
140 9.9 1.1 1.0 40.7 2.3 2.5 10.5 1.3 1.0
3.1 0.3 0.4 10.6 0.5 0.8 2.2 0.3 0.4
160 10.2 1.2 0.6 38.4 2.6 1.8 9.4 1.3 0.9
2.7 0.3 0.6 11.8 0.6 1.0 2.4 0.3 0.5
180 3.1 0.3 0.5 10.0 0.9 1.2 2.7 0.3 0.5
8.9 1.2 0.8 33.2 2.6 2.5 8.4 1.4 1.1
2.8 0.4 0.8 7.9 0.4 1.6 2.3 0.3 0.4
Long S, longitudinal strain; Long Sr, longitudinal strain rate; Rad S, radial strain; Rad Sr, radial strain rate; Circ S, circumferential strain; Circ Sr, circumferential strain rate.
significantly shortened at 160 bpm compared with that at 120 bpm (P < 0.001). In contrast, left atrial dimension, LV internal dimension in systole and diastole, and SV were not significantly different at different HRs.
shown in Table 3. The peak early diastolic torsion rate at 180 bpm was significantly increased compared with that at 120 bpm (P ¼ 0.003). Plots of individual dogs’ peak early diastolic torsion rate are shown in Figure 1. Other deformation parameters in diastole were not significantly different.
2D-STE All myocardial segments for short-axis and long-axis speckle tracking images were included in the statistical analysis. The coefficient of variation (minimumemaximum) of intraobserver 2D-STE measurements were 0.2e13.5% for radial deformations, 0.2e10.1% for circumferential deformations, 0.1e17.1% for longitudinal deformations, and 0.7e16.6% for torsional motions. The results of systolic and diastolic myocardial strain and strain rate variables using 2D-STE at different HRs are shown in Table 2. All strain and strain rate variables were not significantly different at the range of 120e180 bpm. The results of systolic and diastolic myocardial torsional variables using 2D-STE at different HRs are
Discussion Multidirectional myocardial deformations could be assessed using 2D-STE to evaluate myocardial function at HRs of 120e180 bpm in healthy anesthetized beagles. Strain and strain rate variables were not changed by increases in HR. However, the torsion rate in early diastole was elevated at an HR of 180 bpm. In this study, strain and strain rate variables in the longitudinal, circumferential, and radial directions were not changed with increasing HR for reasons incompletely understood. Possibly, LV performance assessed using strain and strain rate
Table 3 Systolic and early diastolic myocardial torsional variables (mean SD) using two-dimensional speckletracking echocardiography at different pacing rates in 13 healthy anesthetized beagle dogs. Variable
HR (bpm) 120
Systolic basal rotation ( ) Systolic basal rotation rate ( /s) Early diastolic basal rotation rate ( /s) Systolic apical rotation ( ) Systolic apical rotation rate ( /s) Early diastolic apical rotation rate ( /s) Systolic torsion ( ) Systolic torsion rate ( /s) Early diastolic torsion rate ( /s) a
2.9 66.8 42.0 9.3 110.8 87.6 8.6 95.5 96.1
140 1.6 31.6 26.7 3.8 44.3 36.1 3.8 40.6 36.0
3.4 75.3 51.5 9.7 121.5 107.4 10.2 106.8 108.2
160 1.9 22.2 36.7 3.2 41.5 27.7 3.1 45.3 43.6
Within a row, the value differs significantly (P < 0.008) from the value at 120 bpm.
4.2 77.1 43.5 8.2 106.6 86.0 10.0 124.7 110.2
180 2.4 24.5 41.3 3.7 50.4 36.5 4.5 58.3 36.4
4.1 83.7 75.9 8.5 124.5 118.0 11.0 136.9 161.9
2.2 23.5 45.6 2.7 56.5 44.7 3.0 40.9 51.3a
144 variables did not change to a sufficiently substantial degree to be detected. These findings are in agreement with those of an earlier study.21 In contrast, the torsion rate in early diastole was elevated at an HR of 180 bpm. LV torsion is reported to reflect the balance of function between the subendomyocardium and subepimyocardium.22 The greater torsional deformation in early diastole observed at higher HR may be caused by a decrease in the myocardial function of the subendomyocardium and an increase in subepimyocardial function in the presence of shortened ejection and filling times. With increasing HR, diastole is reduced more than systole. Because coronary blood flow to the endomyocardium mainly occurs in diastole,23 subendomyocardial function may be affected more compared to that of the subepimyocardium with increasing HRs. Furthermore, because both the subepimyocardium and subendomyocardium work together to produce a nearly homogenous transmural distribution of myocardial stress and fiber strain during ejection,24 a decrease in subendomyocardial function may be compensated by an increase in subepimyocardial function. Therefore, decreased myocardial function in the subendomyocardium combined with a compensatory increase in subepimyocardial function could be the cause for the greater torsional deformation observed at an HR of 180 bpm. The left ventricle isovolumic contraction and relaxation times decrease with increasing HR. Moreover, diastole, and thus the relaxation component, is more influenced by increasing HR than systole. Isovolumic contraction is a dynamic process characterized by layer-dependent deformations.25 The dynamic interaction between subendomyocardial and subepimyocardial fiber helices in the LV according to each layer-
R. Suzuki et al. dependent contraction leads to a twisting motion.26 Furthermore, the potential energy stored in the twisted LV is rapidly released in early diastole, leading to swift recoil of the LV during isovolumic relaxation.22 The details of myocardial function in this phase of the cardiac cycle have not been assessed non-invasively using conventional echocardiography. In this study, the torsion rate in early diastole was elevated at an HR of 180 bpm. In accordance with the findings of earlier studies27e29 and based on the fact that LV torsion is determined by the orientation of the helical myocardial fibers,30,31 the early diastolic torsion rate might reflect enhanced myocardial relaxation and may provide additional non-invasive insight into LV diastolic function, particularly during the isovolumic period. LV torsion is thought to be a mechanism by which the ventricle equalizes transmural oxygen demand gradients, thus minimizing oxygen consumption and optimizing myocardial energetics and efficiency.32e34 The increase in the diastolic torsion rate associated with high HR suggests an improvement of the LV ability to modulate transmural metabolic gradients, which might result in SV maintenance against shortened ejection and filling times. Our study has several limitations. The small number of dogs may affect the statistical power and limit extrapolation of our findings to larger populations. Because of the study design, the effects of anesthesia on myocardial function could not be eliminated. Therefore, our findings should not be extrapolated to conscious dogs. Calculation of LV torsion depends on non-simultaneous measurements of two segments (base and apex), which may have affected our results. In addition, myocardial rotation is reported to be dependent on transducer angulation35 and the true apex of the left ventricle needed for 2D-STE analysis might not be technically acquirable. Speckle imaging as determined by three-dimensional echocardiography in a future study may resolve these limitations. Only normal dogs were examined, however myocardial function assessed by 2D-STE may vary between normal and failing remodeled hearts. Finally, future work incorporating pressure-volume loop analysis for a more accurate evaluation of cardiac function is warranted.
Conclusions Figure 1 Plots of individual dogs’ peak early diastolic LV torsion rate assessed by two-dimensional speckletracking echocardiography at the pacing rates of 120, 140, 160, and 180 bpm.
Myocardial deformations were assessed using 2DSTE at HRs between 120 and 180 bpm in healthy anesthetized beagles. Torsion rate in early diastole
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was elevated only at 180 bpm HR, which may reflect increased myocardial relaxation with increasing HR. Enhanced LV torsion at higher HR may play an important role in preserving SV in the presence of shortened ejection and filling times. Although further studies are needed, 2D-STE examinations of myocardial deformations might provide important noninvasive information on myocardial contractile function.
deformation, but depressed longitudinal and radial deformation in patients with diastolic heart failure. Eur Heart J 2008;29:1283e1289. Mizuguchi Y, Oishi Y, Miyoshi H, Iuchi A, Nagase N, Oki T. The functional role of longitudinal, circumferential, and radial myocardial deformation for regulating the early impairment of left ventricular contraction and relaxation in patients with cardiovascular risk factors: a study with twodimensional strain imaging. J Am Soc Echocardiogr 2008; 21:1138e1144. Lim P, Mitchell-Heggs L, Buakhamsri A, Thomas JD, Grimm RA. Impact of left ventricular size on tissue Doppler and longitudinal strain by speckle tracking for assessing wall motion and mechanical dyssynchrony in candidates for cardiac resynchronization therapy. J Am Soc Echocardiogr 2009;22:695e701. Jacobs G, Mahjoob K. Influence of alterations in heart rate on echocardiographic measurements in the dog. Am J Vet Res 1988;49:548e552. Yamamoto K, Masuyama T, Tanouchi J, Doi Y, Kondo H, Hori M, Kitabatake A, Kamada T. Effects of heart rate on left ventricular filling dynamics: assessment from simultaneous recordings of pulsed Doppler transmitral flow velocity pattern and haemodynamic variables. Cardiovasc Res 1993; 27:935e941. Crosara S, Borgarelli M, Perego M, Ha ¨ggstro ¨m J, La Rosa G, Tarducci A, Santilli RA. Holter monitoring in 36 dogs with myxomatous mitral valve disease. Aust Vet J 2010;88: 386e392. Rishniw M, Erb HN. Evaluation of four 2-dimensional echocardiographic methods of assessing left atrial size in dogs. J Vet Intern Med 2000;14:429e435. Sahn DJ, DeMaria A, Kisslo J, Weyman A. Recommendations regarding quantitation in M-mode echocardiography: results of a survey of echocardiographic measurements. Circulation 1978;58:1072e1083. Schober KE, Hart TM, Stern JA, Li X, Samii VF, Zekas LJ, Scansen BA, Bonagura JD. Detection of congestive heart failure in dogs by Doppler echocardiography. J Vet Intern Med 2010;24:1358e1368. Nagueh SF, Appleton CP, Gillebert TC, Marino PN, Oh JK, Smiseth OA, Waggoner AD, Flachskampf FA, Pellikka PA, Evangelista A. Recommendations for the evaluation of left ventricular diastolic function by echocardiography. J Am Soc Echocardiogr 2009;22:107e133. Teshima K, Asano K, Sasaki Y, Kato Y, Kutara K, Edamura K, Hasegawa A, Tanaka S. Assessment of left ventricular function using pulsed tissue Doppler imaging in healthy dogs and dogs with spontaneous mitral regurgitation. J Vet Med Sci 2005;67:1207e1215. Lewis JF, Kuo LC, Nelson JG, Limacher MC, Quinones MA. Pulsed Doppler echocardiographic determination of stroke volume and cardiac output: clinical validation of two new methods using the apical window. Circulation 1984;70: 425e431. Weidemann F, Jamal F, Sutherland GR, Claus P, Kowalski M, Hatle L, De Scheerder I, Bijnens B, Rademakers FE. Myocardial function defined by strain rate and strain during alterations in inotropic states and heart rate. Am J Physiol Heart Circ Physiol 2002;283:H792eH799. Takeuchi M, Otsuji Y, Lang RM. Evaluation of left ventricular function using left ventricular twist and torsion parameters. Curr Cardiol Rep 2009;11:225e230. Domalik-Wawrzynski LJ, Powell Jr WJ, Guerrero L, Palacios I. Effect of changes in ventricular relaxation on early diastolic coronary blood flow in canine hearts. Circ Res 1987;61:747e756.
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Conflicts of interest None.
Acknowledgments
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The authors wish to thank Syo Miyazawa and Tetsuya Uematsu for their technical assistance. 14.
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