|Year : 2018 | Volume
| Issue : 3 | Page : 270-276
Left ventricular untwist in patients with diastolic dysfunction: speckle tracking imaging study
Mahmoud A Soliman, Mahmoud K Ahmed, Morad B Mena, Mohamed S.S Montaser
Members of Menoufia Cardiology Department, Faculty of Medicine, Egypt
|Date of Submission||25-Jun-2018|
|Date of Acceptance||17-Jul-2018|
|Date of Web Publication||07-Jan-2019|
Dr. Mohamed S.S Montaser
Shebin El Koum, Menoufia Governorate, 32511
Source of Support: None, Conflict of Interest: None
Background There is no single noninvasive index that can directly assess diastolic function. Untwist contributes to diastolic suction and early filling. Speckle tracking imaging (STI) can be used to study the relation between diastolic indices and untwist in patients with diastolic dysfunction.
Patients and methods A total of 75 patients with diastolic dysfunction and 25 normal volunteers were selected for this study. According to mitral flow pattern, the patients were classified into group I (abnormal relaxation), group II (pseudonormalized), and group III (stiffness pattern). Using STI, the basal and apical short-axis views were imaged. Stored data were processed to get apical and basal rotation, systolic twist, peak systolic twist ratio, diastolic untwist ratio, and time to peak twist and untwist ratio.
Results Peak untwisting ratio was significantly higher in Group I Patients that decreased to be normalized and even decreased with progression of diastolic dysfunction from Group II to Group III. There was a highly significant positive and negative correlation with end-diastolic volume and end-systolic volume, respectively. Time to peak untwist ratio nonsignificantly increased from group I to III, with nonsignificant correlation between untwist ratio and peak E, A, and E/A ratio.
Conclusion Patients with relaxation abnormality have a higher untwist ratio, which decreases gradually with progression from relaxation to stiffness pattern. It may appear as a compensatory mechanism to ensure early filling with relaxation abnormality.
Keywords: diastolic dysfunction, left ventricular twist and untwist, speckle tracking imaging, untwist ratio
|How to cite this article:|
Soliman MA, Ahmed MK, Mena MB, Montaser MS. Left ventricular untwist in patients with diastolic dysfunction: speckle tracking imaging study. Benha Med J 2018;35:270-6
|How to cite this URL:|
Soliman MA, Ahmed MK, Mena MB, Montaser MS. Left ventricular untwist in patients with diastolic dysfunction: speckle tracking imaging study. Benha Med J [serial online] 2018 [cited 2020 May 28];35:270-6. Available from: http://www.bmfj.eg.net/text.asp?2018/35/3/270/249413
| Introduction|| |
The physiological hallmarks of left ventricular (LV) diastolic dysfunction are impaired relaxation, loss of restoring forces, reduced diastolic compliance, and elevated LV filling pressure. LV diastolic dysfunction in clinical practice is generally diagnosed by imaging, and there is no single noninvasive index that provides a direct measure of relaxation, restoring forces, compliance, or LV filling pressure . However, by using a combination of different noninvasive indexes, it is feasible in most patients to determine if diastolic function is normal or impaired .
In clinical practice, to identify and stratify patients with LV diastolic dysfunction, echocardiographic assessment of LV filling using pulsed-wave Doppler flow velocity of the LV inflow in conjunction with pulmonary venous flow and mitral annulus velocity measurements using Doppler tissue imaging (DTI) has been used ,. However, all these indices are load-dependent, measuring events that occur after mitral valve opening (MVO), thus provide little information on the relaxation process that predominantly occurs before MVO, and evaluating only the later stages of LV relaxation . Therefore, novel noninvasive methods for assessing the earlier stages of LV diastole (relaxation and restoring forces) need to be developed .
Systolic LV twisting and early diastolic LV untwisting are key components of normal ventricular function and appear to play important roles in physiological ventricular adaptation and development of clinically relevant cardiovascular disease. Untwist is associated with the release of restoring force and contributes to diastolic suction, which facilitates early LV filling .
Considerable additional work is needed to fully define all aspects of LV twist and untwist mechanics and to determine their role in the assessment of normal and diseased heart . Speckle tracking imaging (STI), a relatively recent modality, enables rapid assessment of LV twist and untwist mechanics, having expanded our understanding of both normal ventricular physiology, adaptation, and decompensated function in key disease states.
| Aim|| |
The aim was to assess the relationship between indices of early diastolic function and untwist in patients with diastolic dysfunction.
| Patients and methods|| |
We prospectively examined 100 individuals [75 patients with different grades of diastolic dysfunction with normal ejection fraction (EF) and 25 normal volunteers], selected from Menoufia University Hospital Outpatients Clinics. They were examined by transthoracic echocardiography for evaluation of dyspnea from January 2016 to January 2018. We included all patients with diastolic dysfunction with normal EF, in sinus rhythm and normal ECG. We excluded any patient having arrhythmia, valvular lesions, history of ischemic heart disease (ECG changes and/or wall motion abnormality), bundle branch block, congenital heart disease, cardiomyopathy, and renal or hepatic disease. Each included patient was subjected to full history taking, thorough clinical examination, 12-lead ECG, and laboratory investigations (kidney function, liver function, complete blood count, blood sugar, serum uric acid, and lipid profile).
Standard echocardiographic examination
Transthoracic echocardiography was done using a commercially available echocardiographic machine (E9; GE Medical Systems, Milwaukee, Wisconsin, USA) according to the recommendations of the American Society of echocardiography . Conventional echocardiography measures left ventricular end diastolic diameter [LVIDd and end-diastolic volume (EDV)], left ventricular end-systolic diameter and volume [LVIDs and end-systolic volume (ESV)], fractional shortening, EF, septal and posterior wall thickness (LVSWT and LVPWT), and LV mass index. Using pulsed-wave Doppler mitral inflow pattern, included patients were classified into three groups: group I included patients with grade 1, abnormal relaxation pattern (E/A ratio<0.8, deceleration time>240 ms, and iso-volumic relaxation time>90 ms); group II included patients with grade II or pseudonormalized filling pattern (0.8<E/A<1.5, deceleration time 140–200 ms, and iso-volumic relaxation time<90 ms) and group III included patients with grade III or restrictive filling pattern (E/A>1.5, deceleration time<140 ms, and iso-volumic relaxation time<70 ms). With pulsed-wave DTI, the septal mitral annular velocity curve was recorded for all patients and control to measure peak E, A, E/A ratio and E/e′.
From the apical four chamber view with the ECG connected to the patient, the time interval between the onset of the QRS on the ECG to the aortic and MVO and closure was measured using pulsed-wave Doppler from the LV outflow and inflow, respectively.
Two-dimensional speckle tracking imaging echocardiography
STI module was used for assessment of LV rotational mechanics through scanning and recording from left para-sternal short-axis view of both basal and apical short-axis planes to quantify basal and apical LV rotations using the same machine and probe, with a probe frequency range 1.7–2.0 MHz at a high frame rate (range: 80–115 frame/s). The basal level was marked as the plane showing the tips of mitral valve leaflets at its center with full-thickness myocardium surrounding the mitral valve. Then the transducer was positioned one or two intercostal spaces more caudal and slightly lateral from the basal site to be perpendicular to the apical imaging plane . The apical level was defined just proximal to the level of LV apical luminal obliteration at the end-systole. The cross-section must be as circular as possible. We have to pay careful attention to ensure that full thickness of myocardium is imaged throughout the cardiac cycle. Three consecutive cardiac cycles were digitally saved in a cine-loop format for later offline analysis . Offline analyses were done by an independent echocardiographer who was not involved in the image acquisition.
To analyze twist and untwist parameters, from the basal and apical short axis, data set with a well-defined endo-cardial border and the regions of interest were adjusted to include all myocardial thickness without including the pericardium. The endocardial borders of both basal and short axis planes were manually traced and subsequently tracked by the software. If poor tracking quality was observed, the region of interest was readjusted until acceptable tracking was obtained, otherwise the segment with poor tracking was discarded and replaced by another one. After processing, curves of basal and apical LV rotation, twist, twist rate, and untwist rate were automatically generated by the software (Excel; Microsoft Corporation, Redmond, Washington, USA). Twist was calculated as apical rotation relative to the basal rotation, with counterclockwise rotation as viewed from LV apex expressed as positive value and clockwise rotation as a negative value. Peak LV twist, peak LV twist rate (as first positive peak after R wave on ECG), and peak LV untwist rate (as the first negative peak after aortic valve closure) were recorded. Cardiac cycle length was measured as R–R interval. Time to peak twist rate was measured as time from R wave to peak twist rate, and time to peak untwist rate was measured as time from R wave to peak untwist rate.
Data were analyzed using SPSS software (SPSS Inc., versions (2015), IBM SPSS Statistics, Developers, IBM corporation, USA). Quantitative data were expressed as mean and SD. Comparative analyses were done using χ2-test, Student t-test, Mann–Whitney U-test, Kruskal–Wallis test, and correlation coefficient test.
| Results|| |
This study included 75 patients proved to have diastolic dysfunction by Doppler mitral flow pattern and 25 normal volunteers. Overall, 33.3% of patients were males and 66.7% were females, with mean age of 50.83±9.27 years, in the study group, compared with 24% males and 76% females, with a mean age of 49.29±11.77 years, in the normal controls. There was no significant difference between patients and controls regarding sex and age (P≥0.05). The prevalence of risk factors (especially hypertension and diabetes) was higher among included patients (P≤0.001). There was a nonsignificant difference regarding conventional echocardiographic parameters (LVIDd, LVIDs, EDV, ESV, and EF) except for a highly significantly higher left atrial diameter in patients than control ([Table 1]).
|Table 1 Demographic and conventional echocardiographic characteristics of studied population|
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There was a significantly higher apical rotation (11.96±8.5 vs. 8.5±4.62 at P≤0.01), systolic twist (16.02±8.34 vs. 11.07±4.83 at P≤0.01), peak untwist ratio (98.74±37.23 vs. 80.87±36.68 at P≤0.01), and peak twist ratio (−128.05±12.88 vs. −119.94±20.98 at P ≤0.03), with nonsignificantly longer time to peak twist (486.44±166.49 vs. 490.36±71.77 at P≥0.05), time to peak twist ratio (98.74±37.23 vs. 80.87±36.68 at P≥0.05), and time to peak untwist ratio (587.5±162.78 vs. 578.16±93.65 at P≥0.05) in patients than controls. There was no difference in basal rotations between patients and controls (−4.59±3.45 vs. −4.56±3.75 at P≥0.05) ([Table 2]).
DTI-derived curve of the septal aspect of the mitral annulus showed that there was a significant progressive decrease of peak septal e wave from group I to groups II and III (7.7±0.03, 7.5±0.03, and 4.9±0.005, respectively at P≤0.05), with a significant decrease of peak a wave (12±0.3, 10±0.02, and 11±0.02, respectively at P≤0.02) together with E/a ratio (0.64±0.29, 0.76±0.21, and 0.68±4.9, respectively at P≤0.01). The E/e as a measure of LV end diastolic pressure showed a highly significant difference among the three groups with progressive increase from group I to group II to group III (8.17±3.2, 9.28±2.49, and 11.78±1.94, respectively at P≤0.01). Regarding isometric relaxation time, there was a nonsignificant progressive increase from group I to group II to group III (71.21±12.88, 77.78±19.08, and 81.4±17.43, respectively, at P≥0.05) ([Table 3]).
|Table 3 Mitral flow Doppler and tissue Doppler imaging parameters among patient subgroups|
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At group level, group I and II patients have a significantly higher apical rotation (14.4±6.6 and 11.4±67 at P≤0.001 and P≤0.07 respectively), peak twist (19.1±6.6 and 15.0±78 vs. 11.07±4.83 at P≤0.001 and P≤0.04 respectively), peak twist ratio (106.4 ±45.2 and 102.4±31.3 vs. 80.87±36.68 at P≤0.04 and P≤0.01, respectively), and peak untwist ratio (139.0±166.8 and −123.60±50.8 vs. −119.94±20.96 at P≤0.001 and P≤0.002, respectively) compared with normal control. However, there was a nonsignificant difference between patients of group III and controls regarding apical rotation (8.7±3.4 vs. 8.51±4.62 at P≥0.05), peak twist (13.3±10.1 vs. 11.07±4.83 at P≥0.05), peak twist ratio (65.6±22.6 vs. 80.87±36.63 at P≥0.050), and peak untwist ratio (−92.1±38.2 vs. −119.94±20.96 at P≥0.05). Basal rotation in group III was significantly lower (−1.8±2.4 vs. −4.56±3.75 at P≤0.02). For time to peak twist (425.0±82.3, 529.7±231.1, 542.4±240.3 Vs 490.36±71.77) and time to peak twist ratio (316.6±114.8, 318±121.8, 364.3±117.1 Vs 347.88±56.05). There was a nonsignificant increase in time with increasing severity of diastolic dysfunction ([Table 4]).
|Table 4 Speckle tracking imaging mode among cases subgroups and controls|
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On doing correlation between peak untwist ratio and conventional echocardiographic parameters, there was a significant positive correlation between both end diastolic diameter and volume (r=023 at P≤0.02 and r=0.22 at P≤0.03, respectively), a statistically significant negative correlation with both end-systolic diameter and volume (r=0.22 at P≤0.03), and a nonsignificant correlation with the other parameters (EF, SV, fractional shortening, and LA diameter) (r=0.18, 0.06, 0.02, and 0.002, respectively, at P≥0.05). However, there was a weak and nonsignificant correlation between untwist ratio and Doppler mitral flow indices (E, A, and E/A) (r=0.06, 0.14, and 0.10, respectively, at P≥0.05) ([Figure 1],[Figure 2],[Figure 3]). The same finding were recorded regarding the correlation between mitral annulus DTI-derived diastolic indices (E, A, E/A, E/e and isometric relaxation time) (r=0.002, 0.050, 004, 0.01 and 0.16, respectively, at P≥0.05) ([Table 5]).
|Table 5 Correlation between untwist parameters with conventional echo, mitral inflow, and mitral annulus TDI parameters|
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| Discussion|| |
This study was based on STE assessment of LV untwist in patients proved to have diastolic dysfunction by transmitral Doppler flow indices to assess the relation between LV untwist and indices of diastolic dysfunction. The major findings of this study were as follows: first, a significantly higher apical rotation, peak twist, peak twist ratio, and peak untwist ratio when all patients were compared with controls; second, a significantly higher apical rotation, peak twist, peak twist ratio, and untwist ratio among group I (impaired relaxation), then these values decreased gradually from group I to group II and III to be normalized or even decreased in group III; third, time to peak twist, twist ratio, and untwist ratio showed a progressive nonsignificant increase; fourth, there was a significantly positive correlation between peak untwist ratio with LVIDd and EDV, with a significantly negative correlation with LVIDs and ESV; and fifth, there was no association or correlation between untwist ratio and peak E, A, and E/A ratio.
Several studies of patients with diastolic dysfunction or heart failure with preserved EF demonstrated that patients’ earlier stages of diastolic dysfunction have a higher untwist and untwist ratio that becomes normalized or decreased with higher grades of diastolic dysfunction, and this findings was not applicable to patients with systolic heart failure ,,.
These findings can be explained as follow. Twisting and untwisting of the LV are important aspects of the cardiac mechanics and function. In a normal heart, the onset of myofiber shortening occurs earlier in the endocardium than the epicardium . During pre-ejection, subendocardial shortening and subepicardial stretch contribute to a brief clockwise rotation of the LV apex and counterclockwise rotation of the base ,. During ejection, the activation and contraction of the subepicardial layer with larger radius of arm of momentum produces higher torque to dominate the direction of rotation, resulting in counterclockwise of the apex and clockwise rotation of the base leading to ventricular twisting. Twisting and shearing of the subendocardial fibers deform the matrix and result in storage of potential energy in the deformed intracellular giant protein titin filaments and in the extracelluar collagen fibers to be converted into kinetic energy (restoring force) with the start of relaxation leading to recoil and untwist in early diastole . In most patients with diastolic dysfunction, the subendocardial layer suffers first and becomes affected earlier leading to a decrease in its counterbalancing effect and the subepicardial domination of rotation becomes more prominent with increased both twist and untwist. With disease progression, the subepicardial layer becomes affected leading to decrease of its domination with progressive decrease of both twist and untwist .
Wang et al.  reported that the LV end systolic volume is an important determinant of untwisting rate in patients with diastolic dysfunction irrespective of LV EF, which is in agreement with the finding of this study. Dong et al.  reported that higher LV EDVs produced higher twist and untwist when ESVs were held constant, and higher LV ESV produced lower twist and untwist when EDVs were held constant. These findings explain the positive correlation between EDV and negative correlation between ESV with ventricular untwist reported in this study.
The absence of correlation between untwist ratio and both mitral inflow and Doppler tissue-derived diastolic parameters can be explained as follow: first, all these indices are load-dependent, measuring events that occur after MVO, thus provide little information on the relaxation process that predominantly occurs before MVO and evaluating only the later stages of LV relaxation . However, untwisting starts in late systole before aortic valve closure, and nearly 50–70% of LV untwisting occurs within the period of isovolumic relaxation before MVO, whereas the rest is completed during early diastolic filling phase , leading to time disassociation between the two events. Second, relaxation and stiffness are the major determinant of mitral flow pattern but relaxation is not the sole determinant of untwist where untwist is controlled mainly by the interaction between relaxation and restoring forces and finally, untwist ends in early diastole and before the effect of stiffness. LV untwisting rate has been associated with early diastolic load and restoring forces but not LV stiffness ,. It becomes clear that the factors controlling mitral flow pattern are not the same that control untwist ratio in addition to different timing of both events. These facts can explain the lack of correlation between both parameters.
Regarding time to peak twist and twist ratios, contractility is a major determinant of twist, and it was proved that patients with diastolic dysfunction have subclinical affection of myocardial contractility despite normal EF . This impaired contractility may be the underlying cause of prolongation of time to peak twist and twist ratio. Regarding time to peak untwist ratio, the prolongation can be explained as follow: first, impaired relaxation tends to prolong time to peak untwist ratio, and second, increased restoring force in patient with impaired relaxation secondary to dominant subepicardial and weakend counterbalancing effect of suendocardial layer in those patients tends to accelerate untwist and shorten the time to peak untwist ratio. The increased restoring force will ameliorate the effect of impaired relaxation and lead to a nonsignificant prolongation of the time to peak untwist ratio ,. With disease progression contractility decreases leading to decrease of restoring force and relaxation becomes more impaired and tends to decrease rate of untwist and prolongation of time to peak untwist ratio; therefore, time prolongation increases with increasing severity of diastolic dysfunction. However, the smaller number in group III (10 patients) was a limiting factor to explore its effect on time to peak untwist ratio.
| Conclusion|| |
Untwist may add a new dimension to the noninvasive assessment of diastolic dysfunction. It actually reflects the mechanical aspect of global diastolic function especially the early phase of diastole responsible for creation of suction to assure efficient early filling. Twist and untwist are a strong bridge between systole and diastole.
The sample size especially in group III was smaller (10 patients). There was heterogeneity in the underlying cause of diastolic dysfunction. Inspite of paying greater attention to locate the exact apical and basal planes, variability may occur between patients and this may affect values of rotations from patient to patient. Apical and basal plane imaging does not occur in the same cardiac cycle. Lastly, out of plane motions especially at basal plane may be a problem. Thus, three-dimensional STE may solve some of these limitations.
I would first like to thank my thesis advisor Professor Mohamed Said Shalaby, Professor of Cardiology, Cardiology Department Faculty of Medicine, Menoufia University. The door to Professor Shalaby’s office was always open whenever I ran into a troubled spot or had a question about my research or writing. He consistently allowed this paper to be my own work but steered me in the right direction whenever he thought I needed it. I would also like to thank the experts who were involved in the validation survey for this research project and the readers of this thesis: Professor Mahmoud A. Soliman, Professor of Cardiology, Cardiology Department, Faculty of Medicine, Menoufia University, and Professor Mahmoud K. Ahmed, Professor of Cardiology, Cardiology Department, Faculty of Medicine, Menoufia University. Without their passionate participation and input, the validation survey could not have been successfully conducted. I would also like to acknowledge Dr Moyrad Beshay Mena, Lecturer of Cardiology, Cardiology Department, Faculty of Medicine, Menoufia University, as the third reader of this thesis, and I am gratefully indebted to his valuable comments on this thesis. Finally, I must express my very profound gratitude to my parents, sisters, and to my wife for providing me with unfailing support and continuous encouragement throughout my years of study and through the process of researching and writing this thesis. This accomplishment would not have been possible without them.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Flachskampf FA, Sørensen TB, Solomon SD, Duvernoy O, Smiseth OA. Cardiac imaging to evaluate left ventricular diastolic function. JACC Cardiovasc Imaging 2015; 8:1071–1093.
Smiseth OA. Evaluation of left ventricular diastolic function: state of the art after 35 years with Doppler assessment. J Echocardiogr 2018; 16:55–64.
Maurer MS, Spevack D, Burkhoff D, Ronzon KI. Diastolic dysfunction: can it be diagnosed by Doppler echocardiography? J Am Coll Cardiol 2004; 44:1543–1549.
Oh JK, Hatle L, Tajik AJ, Little WC. Diastolic heart failure can be diagnosed by comprehensive two-dimensional and Doppler echocardiography. J Am Coll Cardiol 2006; 47:500–506.
Dong S, Hees P, Siu C, Weiss J, Shapiro E. MRI assessment of LV relaxation by untwisting rate: a new isovolumic phase measure of tau. Am J Physiol Heart Circ Physiol 2001; 281:H2002–H2009.
Takeuchi M, Borden WB, Nakai H, Nishikage T, Kokumai M, Nagakura T, Otani S, Lang RM. Reduced and delayed untwisting of the left ventricle in patients with hypertension and left ventricular hypertrophy: a study using two-dimensional speckle tracking imaging. Eur Heart J 2007; 28:2756–2762.
Stöhr EJ, Shave RE, Baggish AL, Weiner RB. Left ventricular twist mechanics in the context of normal physiology and cardiovascular disease: a review of studies using speckletracking echocardiography. Am J Physiol Heart Circ Physiol 2016; 311:H633–H644.
Mor-Avi V, Lang RM, Badano LP, Belohlavek M, Cardim NM, Derumeaux G et al.
Current and evolving echocardiographic techniques for the quantitative evaluation of cardiac mechanics: ASE/EAE consensus statement on methodology and indications endorsed by the Japanese Society of Echocardiography. J Am Soc Echocardiogr. 2011; 24:277–313.
Hollekim-Strand SM, Hoydahl SF, Follestad T, Dalen H, Bjørgaas MR, Wisløff U et al.
Exercise training normalizes timing of left ventricular untwist rate, but not peak untwist rate, in individuals with type 2 diabetes and diastolic dysfunction: a pilot study. J Am Soc Echocardiogr 2016; 29:421–430.
Maufaris C, Schuster I, Doucende G, Vitiello D, Rupp T, Dauzat M et al.
Endurance training minimizes age-related changes of left ventricular twist-untwist mechanics. J Am Soc Echocardiogr 2014, 27:128–1215.
Park SJ, Miyazaki C, Bruce CJ, Ommen S, Miller FA, Oh JK. Left ventricular torsion by two-dimensional speckle tracking echocardiography in patients with diastolic dysfunction and normal ejection fraction. J Am Soc Echocardiogr 2008; 21:1129–1137.
Wang J, Khoury DS, Yue Y, Torre-Amione G, Nagueh SF. Left ventricular untwisting rate by speckle tracking echocardiography. Circulation 2007; 116:2580–2586.
Wang J, Khoury DS, Yue Y, Torre-Amione G, Nagueh SF. Preserved left ventricular twist and circumferential deformation, but depressed longitudinal and radial deformation in patients with diastolic heart failure. Eur Heart J 2008; 29:1283–1289.
Ashikaga H, van der Spoel TI, Coppola BA, Omens JH. Transmural myocardial mechanics during isovolumic contraction. JACC Cardiovasc Imaging. 2009; 2:202–211.
Sengupta PP, Tajik AJ, Chandrasekaran K, Khandheria BK. Twist mechanics of the left ventricle: principles and application. JACC Cardiovasc Imaging 2008; 1:366–376.
Fukuda N, Terui T, Ishiwata S, Kurihara S. Titin-based regulation of diastolic and systolic functions of mammalian cardiac muscle. J Mol Cell Cardiol 2010; 48:876–881.
Nakatani S. Left ventricular rotation and twist: why should we learn? J Cardiovasc Ultrasound 2011; 9:1–6.
Dong SJ, Hees PS, Siu CO, Weiss JL, Shapiro EP. MRI assessment of LV relaxation by untwisting rate: a new isovolumic phase measure of tau. Am J Physiol Heat Circ Physiol 2001; 281:H2002–H2009.
Burns AT, La Gerche A, MacIsaac AI, Prior DL. Augmentation of left ventricular torsion with exercise is attenuated with age. J Am Soc Echocardiogr 2008; 21:315–320.
Opdahl A, Remme EW, Helle-Valle T, Edvardsen T, Smiseth OA. Myocardial relaxation, restoring forces, and early-diastolic load are independent determinants of left ventricular untwisting rate. Circulation 2012; 126:1441–1451.
Humg CL, Hou CL, Hu GC, Kuo JY, Hsu CY, Tsai CH et al.
Myths and facts about heart failure with preserved ejection fraction: risk factors, longevity, potential pharmacological and exercise interventions. Int J Gerontol 2013; 7:1–7.
[Figure 1], [Figure 2], [Figure 3]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5]