Assessment of longitudinal systolic function using tissue motion annular displacement in healthy dogs - J Vet Cardiol. 2018 Jun;20(3):175-185
Wolf M., Lucina S.B., Brüler B.C., Tuleski G.L.R., Silva V.B.C., Sousa M.G.Assessment of longitudinal systolic function using tissue motion annular displacement in healthy dogs.J Vet Cardiol. 2018 Jun;20(3):175-185.
INTRODUCTION: Left ventricular systolic function is one of the main parameters studied in echocardiography. Longitudinal systolic function, however, is less commonly evaluated in routine examinations but may provide early information on systolic dysfunction. The movement of the mitral annulus toward the apex has already been determined as a method for evaluation of longitudinal systolic function in dogs, but the study of this movement by speckle tracking with the tissue motion annular displacement (TMAD) technique has not yet been evaluated.
ANIMALS: One hundred fifty-three client-owned healthy dogs.
METHODS: Cross-sectional study. One hundred fifty-three client-owned healthy dogs underwent physical examination, electrocardiography, blood pressure measurement, and a standard and speckle tracking echocardiography. Systolic function was evaluated by global longitudinal strain (GLS) and TMAD. These parameters were compared with the standard echocardiographic data.
RESULTS: A correlation was found between GLS, TMAD, and body weight. Tissue motion annular displacement and GLS were significantly correlated (p < 0.001) with other surrogates of systolic function, including ejection fraction and fractional shortening. There were no differences in TMAD between sexes. The coefficient of variation (CV) of the intraobserver evaluation in the global TMAD (CV 4.44) was slightly higher than that in the GLS (CV 3.74). Also, TMAD was not influenced by heart rhythm and could be acquired more rapidly than GLS.
CONCLUSIONS: Tissue motion annular displacement is a rapid and reproducible method for the assessment of left ventricle longitudinal function in healthy dogs. However, more studies are needed to validate the real clinical applicability of TMAD in animals with heart diseases.
- AP4 apical 4-chamber
- AP2 apical 2-chamber
- BSA body surface area
- BW body weight
- EF ejection fraction
- FS fractional shortening
- GLS global longitudinal strain
- HR heart rate LSt longitudinal strain
- MAM mitral annulus motion
- ROI region of interest
- SBP systolic blood pressure
- TMAD tissue motion annular displacement
Left ventricular systolic function may be evaluated by measurement of several parameters in conventional echocardiography . However, measurements such as fractional shortening (FS) and ejection fraction (EF) obtained by M-mode specifically evaluate the circumferential myocardial fibers. It is thought that ventricular contraction is mainly driven by circumferential myocardial fibers [2,3], but longitudinal fibers also play a relevant role in systole [4,5].
Interestingly, Jones et al.  reported that the longitudinal myocardial fibers are the first to be impaired in systolic dysfunction. In dogs, standard echocardiography provides information on systolic function using parameters that are known to be affected by volume overload, as well as being highly influenced by the operator’s experience and image quality [7,8]. Thus, evaluation of longitudinal fibers may assist in echocardiographic assessment of systolic function. In addition to the conventional assessment of systolic function by standard echocardiography, several echocardiographic techniques are used to evaluate the longitudinal systolic function in dogs.
The difference of the mitral annular displacement in systole and diastole obtained by M-mode in septal and lateral parts of the mitral annulus corresponds to the mitral annulus motion (MAM), a technique that provides information on long axis’ systolic function . Also, the longitudinal shortening fraction is another method of evaluation of the longitudinal contraction which can be acquired by the ratio between MAM and left ventricular internal dimension at end-diastole obtained from the apical 4-chamber (AP4) view . Other techniques obtained by speckle tracking, such as longitudinal strain (LSt) and strain rate, have also been investigated in dogs and evaluate the percentage of myocardial deformation and the velocity of such deformation [11e14].
Recent studies in man have shown that tissue motion annular displacement (TMAD) is a rapid technique that is less dependent on high-definition imaging and significant operator experience when compared with measurement of EF [15,16]. Moreover, tissue motion annular displacement provides information on systolic function encompassing longitudinal fibers by the degree of displacement of the annulus toward the apex. Tissue motion annular displacement of the mitral valve is obtained from the definition of three regions of interest (ROIs): two in the mitral annulus and one at the apex of the left ventricle and provides information of longitudinal systolic function based on the distance of the excursion of the points of the mitral annulus toward the cardiac apex during systolea .
At least in people, tissue motion annular displacement is believed to allow the early diagnosis of systolic dysfunction because individuals with early systolic impairment may have a preserved EF when evaluated with conventional echocardiography, although the TMAD may already be reduced . Because a compensatory increase in circumferential shortening can maintain normal systolic indices despite the decreased longitudinal systolic function, a multidirectional myocardial evaluation might be rewarding for diagnostic purposes [15,17,18].
Interestingly, although other techniques that evaluate the distance of mitral annular displacement during systole have already been studied, to the author’s knowledge, the speckle tracking TMAD technique has never been investigated in dogs. The purposes of this study were threefold: (1) to evaluate the longitudinal systolic function in healthy dogs by tissue motion annular displacement; (2) to investigate whether a correlation exists between TMAD and either the global longitudinal strain (GLS) or other systolic function parameters derived from conventional echocardiography; and (3) to determine if TMAD is influenced by age, sex, body weight (BW), heart rate (HR), or cardiac rhythm. Materials and methods Animals The cross-sectional observational study included 153 client-owned healthy dogs of various breeds and ages enrolled prospectively between October 2016 and April 2017 at the cardiology section of a veterinary teaching facility. All dogs underwent a thorough physical examination, blood pressure assessment, electrocardiography and echocardiography. Systolic blood pressure (SBP) was measured indirectly in all dogs by trained observers (M.W., S.B.L.) using the Doppler technique, as described elsewhere .
Several measurements were taken over 5e10 min to obtain an average of five values of stable measurements. Also, a 3-min computerbased electrocardiogramb was recorded immediately before echocardiography in all animals. Hypertensive animals (defined as systolic arterial blood pressure >150 mmHg), as well as dogs with non-sinus arrhythmias, acquired or congenital heart diseases, and cardiac neoplasms, were excluded from this investigation. All procedures were previously approved by the Institutional Animal Care and Use Committee (protocol 072-2016) and complied with the National Institutes of Health Guide for the Care and Use of Laboratory Animals. Echocardiography The echocardiographic examinationc was performed in all animals without sedation, with the dogs positioned in left and right lateral recumbency in accordance with the recommendations of the Echocardiography Committee of the Specialty of Cardiology of the American College of Veterinary Internal Medicine .
All echocardiographic examinations and measurements were performed by the same operator (M.W.) and included FS and EF (calculated by the Teichholz formula) obtained by M-mode from the right parasternal short-axis images. Two-dimensional short-axis images obtained from the right parasternal window were used to calculate the left atrium-to-aorta ratio. From the left apical 5-chamber view, pulsed wave Doppler between the transmitral flow and the aortic flow was used to record the isovolumic relaxation time.
Left AP4 view was used to record peak early (E) and late (A) diastolic mitral inflow velocities and the E/A ratio. Tissue Doppler was used to measure the mitral annular early diastolic (E’), late diastolic (A’) velocity, and E’/A’ ratio. Also, the aortic valve closure time (R to AV closure) was documented from the apical 5-chamber image (left ventricular outflow) and corresponded to the time from the beginning of the QRS complex to the end of the aortic valve spectra, which were obtained with the pulsed Doppler gate positioned distal to the aortic valves. That time, in milliseconds, was required for obtaining both the peak systolic longitudinal strain and tissue motion annular displacement. Longitudinal strain During transthoracic echocardiographic examination, two-dimensional AP4 and apical 2-chamber (AP2) images (Fig. 1) were obtained for at least five cardiac cycles from the left parasternal window. The echocardiographic equipment softwared automatically detected the left ventricular myocardium to be screened. Manual corrections were made only a few times when the automatic tracking of the software was obviously incorrect. The LSt was determined in the AP4 and AP2 views as a percentage of left ventricle myocardial deformation in a heartbeat. The GLS was calculated as follows: GLS ¼ ðLSt AP4 þ LSt AP2Þ=2 Tissue motion annular displacement The TMAD was calculated in both the 4- and 2- chamber apical echocardiographic images (Fig. 1) obtained from the left parasternal window using a two-dimensional strain-based tissue tracking technique. Two ROIs were defined: at the origin of the mitral valve leaflets at the septal and lateral parts for the AP4 view or at the anterior and inferior parts of the mitral annulus for the AP2 view.
Figure 1 Longitudinal strain is determined by the software in 4-chamber (A) and 2-chamber (B) images. The mean of both results represents the global longitudinal strain (GLS). Tissue motion annular displacement is automatically determined by the software. However, the operator needs to identify three points: medial and lateral mitral annulus and left ventricular epicardial apex in both 4-chamber (C) and 2-chamber (D) images.
The third ROI was set at the epicardial region of the apex of the left ventricle. After setting the ROIs, tracking was performed automatically by the equipment software. The degree of motion was automatically calculated as the base-to-apex displacement of both annulus (in mm), the midpoint that is determined virtually between the two ROIs of the mitral annulus (in mm), and a percentage value (%) of the midpoint in relation to the total length of the left ventricle. The global TMAD was calculated in four different ways: global TMAD (mm) is the mean of the midpoint value, global tissue motion annular displacement (%) is the mean of the percentage value of midpoint in the AP4 and AP2 chambers view, TMAD (mm/m2 ) is global TMAD (mm) index to body surface area (BSA), and the cube root BW-indexed TMAD (mm/kg) as previously described .
Indexing by BSA was performed according to the following formula: BSA ¼ K body weight in grams2=3 104 K ¼ constantð10:1 for dogsÞ Intraobserver and interobserver variability and time requirements For the repeatability study, 20 animals were randomly reassessed of previously obtained images with a minimum interval of 30 days from the first evaluation by the same observer to calculate the intraobserver variability. The same studies were examined by a coinvestigator (M.G.S.), who was blinded to the results of the first investigation, to measure interobserver variability. The required time for off-line analyses (without image acquisition time) for both strain imaging and TMAD was documented from another 20 studies. Statistical analysis The normality of the data was investigated using the ShapiroeWilk test.
Because the data were nonparametric, the results are presented as the median (interquartile range). For TMAD and LSt analyses, dogs were divided into BW quartiles, which were compared with the KruskaleWallis test, followed by the post hoc Dunns test. The same test was used to investigate differences in tissue motion annular displacement in accordance with cardiac rhythm, while the comparison between results obtained for males and females was obtained by ManneWhitney test. ManneWhitney test was also used to compare the time (in seconds) for off-line analyses of GLS and TMAD. Spearman’s test was used to investigate correlations with ages, SBP, and HR obtained from resting electrocardiogram recordings immediately before the echocardiographic examination, as well as to correlate TMAD, LSt, and the regular echocardiographic data. Also, coefficients of variation were calculated to assess intraobserver and interobserver measurements. All statistical analyses were performed with either the software GraphPad Prisme or Microsoft Excel. A p value < 0.05 was considered significant.
A total of 153 dogs were recruited for this study. The population included small- to large-sized dogs, including Australian Cattle Dog, Chow Chow, Cocker, Boxer, Golden Retriever, Siberian Husky, Great Dane, Collie, Chihuahua, Maltese, Pekingese, Samoyed (n ¼ 1 each), beagle (n ¼ 20), Border Collie (n ¼ 2), French Bulldog (n ¼ 8), dachshund (n ¼ 4), Doberman Pinscher (n ¼ 2), Jack Russell Terrier (n ¼ 2), Labrador Retriever (n ¼ 6), Lhasa Apso (n ¼ 9), German Shepherd (n ¼ 7), Malinois Shepherd (n ¼ 2), Miniature Pinscher (n ¼ 2), American Pit Bull Terrier (n ¼ 2), poodle (n ¼ 4), Pug (n ¼ 2), Rottweiler (n ¼ 3), schnauzer (n ¼ 8), Shih Tzu (n ¼ 2), Whippet (n ¼ 3), Yorkshire (n ¼ 6), and crossbreed dogs (n ¼ 47). Fifty-five dogs (35.9%) were male, and 98 (64.1%) were female. The animals were aged between 4 and 192 months (mean 54.3; median 36), while BW ranged from 1.7 to 50 kg (mean 15.4; median 11.6).
The most observed cardiac rhythm was sinus arrhythmia (52.3%) followed by sinus rhythm (41.2%) and sinus tachycardia (6.5%). Both tissue motion annular displacement and LSt varied in accordance with the size of the animals. Differences were documented when BW quartiles were compared, and the proposal of the values for each quartile is shown in Table 1. Our results show a negative correlation between BW and GLS, which contrasts with the greater displacement of the mitral annulus (in mm) in heavier dogs (Table 1, Fig. 2).
Figure 2 Median and individual values of global tissue motion annular displacement (TMAD; mm) (A) and global longitudinal strain (GLS) (B) obtained in dogs subdivided according to body weight.
However, when the LSt was compared with either the indexed TMAD or the TMAD percent, positive correlations were found to exist (Fig. 3). There was no correlation between the BSAindexed TMAD (mm/m2 ) with regard to sex, SBP, and HR. However, the cube root BW-indexed TMAD (mm/kg) was significantly correlated with HR (R: 0.1730; p: 0.0330), whereas GLS was not (R: 0.0426; p: 0.6009).
Both the BSA-TMAD (mm/m2 ) and the cube root BW-TMAD correlated significantly with several echocardiographic surrogates of volume, contractility, and diastolic function, while the GLS correlated with FS, EF, and isovolumic relaxation time (Table 2). Global longitudinal strain was influenced by cardiac rhythm (p: 0.02), whereas global TMAD (mm) was not (p: 0.37). Animals with sinus arrhythmia (median GLS 23.3 [20.8e25.3]) had higher GLS values than animals with sinus tachycardia (20.7 [19.4e23.2]) and sinus rhythm (21.3 [18.5e25]). Also, tissue motion annular displacement was shown to be a straightforward technique as compared with LSt.
When the time needed to perform the off-line analyses of either technique was compared, the median time for TMAD was less than the required time for strain analyses in both AP4 (TMAD:19.7s; LSt:43.5s) and AP2 (TMAD:18.9s; LSt:40.1s) images. Interobserver and intraobserver repeatability analyses showed good coefficients. TMAD demonstrated either reliability in both intraobserver (coefficient of variation [CV] 4.44) and interobserver (CV 4.12) analyses.
The coefficients of variation of the TMAD were slightly higher than those in the LSt in the interobserver and intraobserver evaluation, except for the comparison of the interobserver GLS in which the GLS (CV 5.2) was higher than the TMAD (CV 4.12).
In this study, tissue motion annular displacement was compared with conventional echocardiography and GLS for the assessment of left ventricle longitudinal systolic function. Conventional echocardiography essentially evaluates radial shortening primarily involving the circumferential myocardial fibers. Echocardiographic parameters obtained by Mmode are commonly used to provide cardiac function information, but the data obtained by this technique show little correlation when compared with invasive methods, especially in dogs with heart disease . In contrast, in conventional echocardiography, the longitudinal myocardial fibers are poorly evaluated .
The contraction of the longitudinal fibers promotes shortening of the left ventricle in the longitudinal direction and consequently, the mitral annulus moves toward the apex . Some techniques performed with conventional echocardiography can be used to evaluate the longitudinal systolic function as well, such as the longitudinal shortening fraction and the MAM [9,10]. Speckle tracking echocardiography is becoming available for general veterinary practice, and several studies have used it to evaluate longitudinal systolic function in healthy dogs [11e14], dogs with mitral valve disease [22e24], induced cardiomyopathy , patent ductus arteriosus , and hyperadrenocorticism , but none of these studies used TMAD as an evaluation technique, at least to our knowledge.
Figure 3 Correlation between global TMAD and GLS. A negative correlation (R:0.2552; p:0.0015) existed when GLS was compared with the global TMAD (mm) (A).
Positive correlations were found when comparing GLS and global tissue motion annular displacement (%) (R:0.5898; p < 0.0001) (B), GLS and global BSA-TMAD (mm/m2 ; R:0.7153; p < 0.0001) (C), and GLS and global cube root BW-indexed TMAD (R:0.4502; p < 0.0001) (D). TMAD, tissue motion annular displacement; GLS, global longitudinal strain; BSA, body surface area; BW, body weight.
Tissue motion annular displacement is a tracking technique that provides information on systolic function from the degree of longitudinal deformation of the mitral annulus , not previously investigated in dogs. Thus, tissue motion annular displacement and GLS are rapid techniques for assessment of longitudinal function, complementing the information obtained from the regular echocardiographic procedure [15,22]. Global longitudinal strain is the sum of myocardial deformations in the longitudinal plane during systole  and provides accurate and angle-independent measurements when compared with magnetic resonance imaging .
Previous studies have determined GLS in healthy dogs [11,13,25]. The GLS recorded by Kusunose et al.  in 25 healthy animals was 18 4%. In our study, higher values were obtained, which are probably related to the greater BW variability of our population. Nonetheless, when we compared our results obtained in dogs with the same BW (21e35 kg), our GLS is similar (18.5%) to that reported by Kusunose et al. Interestingly, the results of this study are in agreement with another study which included a more heterogeneous population, in terms of weight and size . Studies show that GLS has a strong correlation with tissue motion annular displacement (mm) in healthy people , in people with hypertrophic cardiomyopathy , and in individuals undergoing hemodialysis .
In this study, a negative correlation existed between GLS and TMAD (mm), probably attributable to the negative relationship between strain and BW. This fact might be explained by the physiological behavior of systolic function in dogs, with decreased systolic indices in large dogs . While heavier animals have lower myocardial deformation [32,33], their larger heart size results in a greater absolute mitral displacement toward the apex . Because the population of this study was heterogeneous, a representative number of large dogs were enrolled. This fact also explains the disagreement with the medical literature because heart size is relatively constant in adult human beings in contrast to the variations seen between dog breeds. Therefore, the proposal values of TMAD are divided in quartiles of BW, as shown in Table 1. To minimize the effect of BW, GLS was then compared with the global TMAD percent and indexed TMAD (mm/m2 and mm/kg, the least being derived from the cube root BW).
In all cases, positive correlations were found to exist. Therefore, despite higher values in mm, the percentage of annular displacement is lower in larger dogs. Similar results were found by Schober and Fuentes  with the MAM technique. A positive correlation of MAM (in cm) with BW was observed, and when MAM was indexed by BSA, a negative correlation was demonstrated. Although our study showed that BW plays a major role in tissue motion annular displacement and LSt, another study found no differences in the LSt between beagle and Cavalier King Charles Spaniel . These contrasting results are explained by the minimal variation in BW in that comparison, which did not include large dogs. Significant correlations were documented between the global TMAD (mm), HR, and SBP. However, when the BSA-indexed TMAD was used, none of these parameters influenced TMAD.
This is an interesting observation, probably attributable to the fact that small dogs are usually more nervous and often have an associated elevation in HR and SBP than larger dogs. Indexing TMAD to BSA removed this bias. A study in dogs with mitral valve disease showed that HR affected strain rate values  possibly because of the compensatory mechanisms in response to disease, which were eliminated in this study as only healthy animals were evaluated. The same effect occurs for systemic arterial blood pressure. Although the increase in afterload was shown to produce lower strain values , no hypertensive dogs were included in this study.
Interestingly, TMAD (mm/m2 ) was not affected by heart rhythm, whereas LSt was higher in animals with sinus arrhythmia. Owing to the high numbers of dogs with sinus arrhythmia, this result might represent another benefit of TMAD over LSt in clinical practice. In this study, a moderate correlation was shown between either GLS or global tissue motion annular displacement (mm, mm/m2 , mm/kg) and left ventricular internal dimension at end-systole and end-diastole (p < 0.001), which indicate they are preload- and afterloaddependent surrogates. Other studies have demonstrated that the increase of preload and the decrease of afterload can directly increase LSt values [22,34]. Future studies in animals with volume and pressure overload might characterize the behavior of TMAD in these circumstances. The weak correlations between the systolic indices obtained from standard echocardiography and either the GLS or the indexed TMAD (mm/m2 or mm/kg) observed in this study are likely to be related to both EF and FS being surrogates of the radial myocardial shortening. Because both are obtained from the left ventricular internal diameter measured in short-axis images, they do not effectively reflect the longitudinal contraction as observed by LSt and TMAD [11,17]. Similar results were obtained in people undergoing hemodialysis  and individuals with structural heart disease, probably due to the fact the TMAD (mm) is a technique with lower error bias, less dependent on image quality than EF [17,30]. In this study, a negative correlation between age and global TMAD was observed.
In people, a physiological decrease in longitudinal contractility has been shown with age progression , but this has not been validated for dogs. The best way to validate these data in dogs would be a prospective evaluation of the same animal with advancing age . Previous studies have shown that TMAD in people and LSt in people and dogs have a low interobserver and intraobserver variability [15,17,22,27,30,31]. In this study, there was a good repeatability between duplicate measurements of tissue motion annular displacement. The fact that TMAD, in contrast with strain and EF, does not require a good definition of endocardial borders probably explains why TMAD was more reliable in these analyses [15,17,31]. This may be particularly important in patients with pulmonary edema, dyspnea, and in situations in which a good echocardiographic images may be difficult to acquire. A study in patients undergoing hemodialysis demonstrated that TMAD cannot provide prognostic information such as likelihood of cardiac death or cardiac events . In contrast, GLS allows the early detection of longitudinal systolic dysfunction in patients with acute myocardial infarction with preserved EF evaluated by magnetic resonance imaging . Future studies in dogs may show the prognostic capacity of TMAD and the GLS in various heart diseases. The results of this study also showed that TMAD is a more rapid technique when compared with LSt .
Tsang et al.  evaluated 118 human patients and found that all TMAD analyses were concluded in less than 10 s. In this study, the median time needed to complete TMAD was less than 20 s, whereas LSt required a median of approximately 45 s. In a single dog, the time required to complete tissue motion annular displacement AP2 analysis was significantly longer (116.3 s). However, in that case, unusually the definition of the lateral mitral annulus was of low quality, and several manual corrections were necessary to allow the software to track the point toward the cardiac apex in an appropriate fashion. Of note, the TMAD technique itself does not impact the overall examination time because the analytical procedure is performed offline. The only exception to the conventional examination is acquiring the AP2 image, which may be performed without difficulties. Subsequently, the analyses performed offline take approximately 20 s each to be performed, being, therefore, a plausible technique to be included in routine examinations. Some limitations of this study must be considered. The animals were considered healthy based on clinical evaluation, echocardiogram, electrocardiogram, and blood pressure measurement.
However, we cannot exclude the possibility of asymptomatic comorbidities that were not identified by specific ancillary examinations. Systemic blood pressure was obtained by a non-invasive method that is not considered the gold standard. The number and variability of animals may be too small to extrapolate the results obtained for all breeds. This study compared TMAD and GLS with the systolic surrogates obtained by conventional echocardiography, which are influenced by several factors. Therefore, the absence of a gold standard non-invasive technique for comparison is a limitation to be considered. In conclusion, global tissue motion annular displacement (%, mm/m2 , and mm/ kg) shows positive correlation with GLS and with several echocardiographic parameters of systolic function. Also, TMAD allowed the assessment of longitudinal systolic function in a very straightforward fashion and with a reliable intraobserver and interobserver repeatability. It is, therefore, a new and promising tool in veterinary cardiology as an alternative to GLS for assessment of longitudinal systolic function.
However, further studies are warranted to validate the real clinical applicability of tissue motion annular displacement in animals with heart diseases. Conflicts of Interest Statement The authors do not have any conflicts of interest to disclose. Acknowledgments The authors are grateful for the financial support provided by Coordenac¸a˜o de Aperfeic¸oamento Pessoal de Nı´vel Superior (CAPES) and Conselho Nacional de Desenvolvimento Cientı´fico e Tecnolo´gico (CNPq).
- Atkins CE, Curtis MB, Mcguirk SM, Kittleson MD, Sato T, Snyder PS. The Use of M-Mode Echocardiography in Determining Cardiac output in dogs with normal, low, and high output states: comparison to thermodilution method. Vet Radiol Ultrasound 1992;33:297e304.
- Wu EX, Wu Y, Tang H, Wang J, Yang J, Ng MC, Yang ES, Chan CW, Zhu S, Lau CP, Tse HF. Study of myocardial fiber pathway using magnetic resonance diffusion tensor imaging. J Magn Reson Imaging 2007;25:1048e57.
- Sengupta PP, Korinek J, Belohlavek M, Narula J, Vannan MA, Jahangir A, Khandheria BK. Left ventricular structure and function - basic science for cardiac imaging. J Am Coll Cardiol 2006;48:1988e2001.
- Aurigemma GP, Silver KH, Priest MA, Gaasch WH. Geometric changes allow normal ejection fraction despite depressed myocardial shortening in hypertensive left ventricular hypertrophy. J Am Coll Cardiol 1995;26: 195e202.
- Bogaert J, Rademakers FE. Regional nonuniformity of normal and adult left ventricle. Am J Physiol Heart Circ Physiol 2001;280:H610e20.
- Jones CJH, Raposo L, Gibson DG. Functional importance of the long axis dynamics of the human left ventricle. Br Heart J 1990;63:215e20.
- Kittleson MD, Eyster GE, Knowlen GG, Bari Olivier N, Anderson LK. Myocardial function in small dogs with chronic mitral regurgitation and severe congestive heart failure. J Am Vet Med Assoc 1984;184:455e9.
- Atkins C, Bonagura J, Ettinger S, Fox P, Gordon S, Ha¨ggstro¨m J, Hamlin R, Keene B, Luis-Fuentes V, Stepien R. Guidelines for the diagnosis and treatment of canine chronic valvular heart disease. J Vet Intern Med 2009;23:1142e50.
- Schober KE, Fuentes VL. Mitral annulus motion as determined by M-mode echocardiography in normal dogs and dogs with cardiac disease. Vet Radiol Ultrasound 2001;42: 52e61.
- Sousa MG, Gava FN, Filho JCS, Silva SNS, Camacho RR, Carareto R, Wolf M, Camacho AA. Long-axis fractional shortening and mitral annulus motion in dogs. Semina Cieˆncias Agra´rias 2016;37:3115e24.
- Chetboul V, Sampedrano CC, Gouni V, Nicolle AP, Pouchelon JL, Tissier R. Ultrasonographic assessment of regional radial and longitudinal systolic function in healthy awake dogs. J Vet Intern Med 2006;20:885e93.
- Wess G, Keller LJM, Klausnitzer M, Killich M, Hartmann K. Comparision of longitudinal myocardial tissue velocity strain, and strain rate measured by two-dimensional speckle tracking and by color tissue Doppler imaging in healthy dogs. J Vet Cardiol 2011;13:31e43.
- Westrup U, McEvoy FJ. Speckle tracking echocardiography in mature Irish Wolfhound dogs: technical feasibility, measurement error and reference intervals. Acta Vet Scand 2013;55:1e11.
- Carnabuci C, Hanas S, Ljungvall I, Tidholm A, Bussadori C, Ha¨ggstro¨m J, Ho¨glund K. Assessment of cardiac function using global and regional left ventricular endomyocardial and epimyocardial peak systolic strain and strain rate in healthy Labrador retriever dogs. Res Vet Sci 2013;95:241e8.
- Suzuki K, Akashi YJ, Mikukoshi K, Kou S, Takai M, Izumo M, Hayashi A, Ohtaki E, Nobuoka S, Miyake F. Relationship between left ventricular ejection fraction and mitral annular displacement by speckle tracking echocardiography in patients with different heart diseases. J Cardiol 2012;60:55e60.
- Tsang W, Ahmad H, Patel AR, Patel AR, Sugeng L, Salgo IS, Weinert L, Mor-Avi V, Lang RM. Rapid estimation of leftventricular function using echocardiographic speckletracking of mitral annular displacement. J Am Soc Echocardiogr 2010;23:511e5.
- Buss SJ, Mereles D, Emami M, Korosoglou G, Riffel JH, Bertel D, Schonland SO, Hegenbart U, Katus HA, Hardt SE. Rapid assessment of longitudinal systolic left ventricular function using speckle tracking of the mitral annulus. Clin Res Cardiol 2012;101:273e80.
- 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 two-dimensional strain imaging. J Am Soc Echocardiogr 2008;21:1138e44.
- Brown S, Atkins C, Bagley R, Carr A, Cowgill L, Davidson M, Egner B, Elliot J, Henik R, Labato M, Littman M, Polzin D, Ross L, Snyder P. Stepien. Guidelines for the identification, evaluation, and management of systemic hypertension in dogs and cats. J Vet Intern Med 2007;21:542e58.
- Thomas WP, Gaber CE, Jacobs GJ. Recommendations for standards in transthoracic Two-Dimensional echocardiography in the dog and cat. J Vet Intern Med 1993;7:247e52.
- Cornell CC, Kittleson MD, Torre PD, Ha¨ggstro¨m J, Lombard CW, Pedersen HD, Vollmar A, Wey A. Allometric scaling of M-mode cardiac measurements in normal adult dogs. J Vet Intern Med 2004;18:311e21.
- Zois NE, Tidholm A, Nagga KM, Moesgaard SG, Rasmussen CE, Ha¨ggstrro¨m J, Pedersen HD, Ablad B, Nilsen HY, Olsen LH. Radial and longitudinal strain and strain rate assessed by speckle-tracking echocardiography in dogs with myxomatous mitral valve disease. J Vet Intern Med 2012;26:1309e19.
- Suzuki R, Matsumoto H, Teshima T, Koyama H. Clinical assessment of systolic myocardial deformations in dogs with chronic mitral valve insufficiency using twodimensional speckle-tracking echocardiography. J Vet Cardiol 2013;15:41e9.
- Mantovani MM, Muzzi RAL, Pereira GG, Yamato RJ, Silva AC, Reis GF, Muzzi LAL, Guimara˜es EC. Systolic cardiac function assessment by feature tracking echocardiography in dogs with myxomatous mitral valve disease. J Small Anim Pract 2015:1e10.
- Kusunose K, Zhang Y, Mazgalev TN, Thomas JD, Popovic ZB. Left ventricular strain distribution in healthy dogs and in dogs with tachycardia-induced dilated cardiomyopathy. J Cardiovasc Ultrasound 2013;11:1e9.
- Spalla I, Locatelli C, Zanaboni AM, Brambilla P, Bussadori C. Echocardiographic assessment of cardiac function by conventional and speckle-tracking echocardiography in dogs with patent ductus arteriosus. J Vet Intern Med 2016;30:706e13.
- Chen HY, Lien YH, Huang HP. Assessment of left ventricular function by two-dimensional speckle-tracking echocardiography in small breed dogs with hyperadrenocorticism. Acta Vet Scand 2014;56:1e10.
- Blessberger H, Binder T. Non-invasive imaging: two dimensional speckle tracking echocardiography: basic principles. Heart 2010;96:716e22.
- Amundsen BH, Helle-Velle T, Edvardsen T, Torp H, Crosby J, Lyseggen E, Stoylen A, Ihlen H, Lima JAC, Smiseth OA, Slordahl SA. Noninvasive myocardial strain measurement by speckle tracking echocardiography. J Am Coll Cardiol 2006;47:789e93.
- Liu L, Tuo S, Zhang J, Zuo L, Liu F, Hao L, Sun Y, Yang L, Shao H, Qi W, Zhou X, GE S. Reduction of left ventricular longitudinal global and segmental systolic functions in patients with hypertrophic cardiomyopathy: study of twodimensional tissue motion annular displacement. Exp Ther Med 2014;7:1457e64.
- Chiu DYY, Abidin N, Hughes J, Sinha S, Kalra PA, Green D. Speckle tracking determination of mitral tissue annular displacement: comparison with strain and ejection fraction, and association with outcomes in haemodialysis patients. Int J Cardiovasc Imaging 2016;32:1511e8.
- Takano H, Fujii Y, Ishikawa R, Aoki T, Wakao Y. Comparison of left ventricular contraction profiles among small, medium and large dogs by use of two-dimensional speckle tracking echocardiography. Am J Vet Res 2010;71:421e7.
- Locatelli C, Spalla I, Zanaboni AM, Brambilla PG, Bussadori C. Assessment of right ventricular function by feature-tracking echocardiography in conscious healthy dogs. Res Vet Sci 2016;105:103e10.
- Weidemann F, Jamal F, Sutherland GR, Sutherland GR, Claus P, Kowalski M, Hatle L, Schherder 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 C 2002;283:H792e9.
- Andersen NH, Poulsen SH. Evaluation of the longitudinal contraction of the left ventricle in normal subjects by Doppler tissue tracking and strain rate. J Am Soc Echocardiogr 2003;16:716e23.
- Fente GJ, Garg P, Foley JRJ, Dobson LE, Musa TA, Erhayiem B, Greenwood JP, Plein S, Swoboda PP. The utility of global longitudinal strain in the identification of prior myocardial infarction in patients with preserved left ventricular ejection fraction. Int J Cardiovasc Imaging 2017;33:1561e9.