European Journal of Echocardiography Advance Access published online on July 29, 2008
European Journal of Echocardiography, doi:10.1093/ejechocard/jen207
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Left ventricular wall segment motion after ultra-endurance exercise in humans assessed by myocardial speckle tracking
1 Research Institute for Sport and Exercise Sciences, Liverpool John Moores University, 15-21 Webster Street, Liverpool L3 2ET, UK
2 Centre for Sports Medicine and Human Performance, Brunel University, UK
3 School of Medicine and Healthcare, University of Leeds, Leeds, UK
4 Department of Chemical Pathology, St George’s Hospital, UK
5 MRC/UCT Research Unit for Exercise Science and Sports Medicine, University of Cape Town, Rondebosch, South Africa
Received 31 March 2008; accepted after revision 5 July 2008.
* Corresponding author. Tel: +44 151 231 4088; fax: +44 151 231 4353. E-mail address: k.george{at}livjm.ac.uk
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Abstract |
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Aims: Assessment of the left ventricular responses to prolonged exercise has been limited by technology available to assess cardiac tissue movement. Recently developed strain and strain rate imaging provide the unique opportunity to assess tissue deformation in all planes of motion.
Methods and results: Nineteen runners (mean ± SD age; 41 ± 9 years) were assessed prior to and within 60 min (34 ± 10 min) of race finish (Comrades Marathon, 89 km). Standard echocardiography assessed ejection fraction and the ratio of early to atrial (E/A) peak transmitral blood flow velocities. Myocardial speckle tracking determined segmental strain as well as systolic and diastolic strain rates in radial, circumferential, and longitudinal planes. Cardiac troponin T (cTnT) assessed cardiomyocyte insult. Ejection fraction (71 ± 5 to 64 ± 6%) and E/A (1.47 ± 0.35 to 1.25 ± 0.30) were reduced (P < 0.05). Peak strain and peak systolic and diastolic strain rates were altered post-race in circumferential (e.g. peak strain reduced from 21.3 ± 2.4 to 17.3 ± 3.2%, P < 0.05) and radial planes. Some individual heterogeneity was observed between segments and planes of motion. A post-race elevation in cTnT (range 0.013–0.272 µg/L) in 5/12 runners did not differentiate changes in LV function.
Conclusion: Completion of the Comrades Marathon resulted in a depression in ejection fraction, E/A, as well as radial and circumferential strain and strain rates. Group data, however, masked some heterogeneity in cardiac function.
Keywords: Cardiac function; Strain; Echocardiography
Recent scientific studies have suggested that prolonged endurance exercise may result in a minor and temporary change in left ventricular (LV) function,1–3 as well as a transient release of cardiac biomarkers.4 Other research has demonstrated a consistent attenuation in right ventricular function in athletes coincident with the presence of ventricular arrhythmia.5 Such studies have raised concern about the impact of individual and/or lifelong participation in prolonged exercise.
Recent research has utilized colour M-mode-derived flow propagation velocities,6 segmental tissue Doppler myocardial velocities,7,8 and tissue Doppler-derived strain and strain rate data3,9 to assess cardiac function after marathon running. The target of these approaches has been to afford a comprehensive assessment of LV function that provides greater insight into case reports of focal necrosis of cardiac tissue in an ultra-endurance athlete,10 segmental wall motion abnormalities reported after prolonged exercise,11,12 or the appearance of clinical signs of heart failure in some ultra-endurance runners.13 Some technical limitations persist, however, including the angle dependency of myocardial velocities, strain and strain rate derived from Doppler images.14 Myocardial speckle tracking provides an alternate method of recording strain and strain rate data which affords no angle dependency and can image LV function in longitudinal, radial, and circumferential planes at multiple levels of the LV.15
We investigated LV function after an ultra-endurance run exercise using myocardial speckle tracking and thus provide segmental analysis of deformation in three planes of motion. We hypothesized that the performance of an ultra-endurance run would result in a depression in LV systolic and diastolic function as assessed by myocardial speckle tracking.
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Subjects
Of 26 runners recruited to the study at the site of race registration, 19 runners [16 males, 3 females, mean ± SD, age=41 ± 9 years (range 29–59), body mass (BM) 71.9 ± 11.3 kg (range 54.0–91.4), height 1.72 ± 0.09 m (range 1.54–1.90)] completed the Comrades Marathon 2005 (distance 89 km from Pietermaritzburg to Durban, South Africa) and made themselves available for post-race testing. All runners provided written informed consent to participate. This study conformed to the standards set by the Declaration of Helsinki and local ethical approval was obtained. Exclusion criteria included any personal and/or early family history of cardiopulmonary disease, including diagnosis and treatment for hypertension, angina, myocardial infarction, and peripheral vascular diseases.
Design
Data were collected at an initial assessment 
24 h prior to the completion of the race. Immediately after race completion, subjects proceeded to a testing area adjacent to the finish within the race medical tent and were reassessed within 60 min of race completion (mean ± SD time from race completion to beginning of scan = 34 ± 10 min). All data collection procedures were administered on both occasions in the same order by the same assessors. All subjects abstained from hard training within the 48 h period prior to pre-testing and avoided caffeine and alcohol consumption 4 h before both assessments. Race conditions were mild with an initial race start temperature of 4°C and a maximal temperature of 24°C. A light southerly breeze was present for most of the race and the cloud cover was scattered.
Procedures and echocardiography
Upon arrival at the testing area, subjects were initially assessed for BM, in running shorts and vest, on standard portable scales (Model A3JJT1K, Hansen, UK). Subjects then lay supine and after a 5 min resting period, duplicate brachial artery systolic and diastolic blood pressures were assessed by standard auscultation. Also, at this time, a resting heart rate was recorded from the ECG within the echocardiography system.
Standard two-dimensional and M-mode echocardiographic scans were performed using a commercially available ultrasound system (Vivid 7, GE Medical, Horton, Norway) with a 1.5–4 MHz phased array transducer. All image acquisitions were made with the subject lying in the left lateral decubitas position. Echocardiograms were obtained from parasternal and apical two- and four-chamber views. All system settings were optimized to produce best signal-to-noise ratio and provide optimal endocardial definition. Measurements obtained included posterior wall thickness at end systole from M-mode recordings at the tip of the mitral valve leaflets. Left ventricular end-diastolic and end-systolic areas were digitized from two-dimensional short-axis sector scans at the level of the mitral valve. Finally, LV end-diastolic volume was assessed via the biplane method from apical scans with all measures performed according to ASE guidelines.16 Ejection fraction, fractional area change, and the end-systolic pressure–volume ratio were estimated LV areas, volumes, and systolic blood pressure. Left ventricular meridonial wall stress,17 an index of afterload, was calculated from M-mode and blood pressure data. Peak blood flow velocities across the mitral valve were determined via Doppler echocardiography. With the mitral annulus maximized and the sample volume placed in the tips of the mitral valve, both early (E) and atrial (A) peak blood flow velocities were recorded and the ratio E/A calculated. From the Doppler trace, deceleration time of the E wave was measured from peak velocity to intersection of the Doppler waveform with baseline.
Radial and circumferential strain data were derived from a parasternal short-axis view imaged at the basal level. Specifically, this was at the level of the first appearance of the superior surface of the papillary muscle when imaged down from the mitral valve to provide a reproducible anatomically landmark for repeat scans. The focal point was positioned close to the centre of the LV cavity to provide optimum beam width while reducing the effects of divergence. The apical window was utilized for longitudinal assessment incorporating apical two- and four-chamber orientations. The focal point was positioned at the level of the mitral valve. In both orientations, frame rates were maximized (>40 and <90 frames per second). All images were optimized with gain, compression, and dynamic range to enhance myocardial definition. Analysis of the two-dimensional images was performed offline using commercially available software (two-dimensional strain, EchoPac, GE Medical, Horton, Norway). Strain and strain rate were derived from continuous frame-by-frame tracking of the natural acoustic speckle markers18 using a block-matching algorithm. Strain and strain rate are calculated from the displacement and rate of displacement of the ‘kernel’.19 Analysis software provided automatic grading of the tracking quality on a scale from 1.0 (optimal) to 3.0 (unacceptable). Segments scoring >2.0 were excluded from the analysis. Visual assessment of tracking quality was also made and segment analysis excluded where appropriate. Radial and circumferential peak strain and peak systolic (S) and diastolic (D) strain rates values were calculated by the software from the following basal myocardial segments, septum, anteroseptum, anterior, lateral, posterior, and inferior walls. Apical images incorporated the whole LV but to correspond to radial and circumferential data only the following segments were analysed: basal septum, basal lateral, basal inferior, and basal anterior walls. An average of four or six segments was used as a global value for longitudinal, circumferential, and radial function. One experienced sonographer was used for all examinations. Images were recorded digitally to magneto optical disc and analysed off-line by a single experienced sonographer. Sonographer specific coefficient of variation data ranged from 4.9 to 7.1% for strain and strain rate derived in radial and circumferential planes. This rose slightly to 7.1–12.7% for indices derived in the longitudinal plane. Pre- to post-race differences in heart rate made it impossible to blind this aspect of analysis. A minimum of three consecutive cardiac cycles were measured and averaged.
In a sub-sample of 10 runners, heart rate was recorded every 5 s during the race via telemetry (Polar, Finland). In 12 runners, whole blood samples were drawn after the echocardiographic examinations. Serum samples were analysed for cardiac troponin T (cTnT) using the third-generation immunoassay (Roche Diagnostics, Lewes, UK). The assay imprecision was 5.5% at 0.32 µg/L and 5.4% at 6 µg/L, had a detection limit of 0.01 µg/L, and an upper limit of 25 µg/L.
Data analysis
Pre- and post-race values for BM, blood pressures, heart rate, standard echocardiogrpahic measures, and mean strain/strain rate data were analysed using repeated measures t-tests. Data for segmental strain/strain rate data from radial, circumferential, and longitudinal planes were analysed via repeated measures two-way ANOVA. Delta (pre–post-race) values for strain and strain rate were correlated with delta heart rate, delta preload, delta afterload, age, and finishing time via Pearson’s Product-Moment analysis. Mean strain and strain rate data were compared via independent t-tests between those runners with and without an elevated cTnT post-race. The critical alpha level was set at 0.05 and all analyses were carried out on Statistica software (Statsoft Ltd, Tulsa, USA). All data are reported as mean ± SD (range).
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Nineteen subjects completed the Comrades Marathon and returned for post-race assessments. A broad spectrum of race finishing times was recorded [586 ± 80 min (range 404–757 min)]. Average heart rate during the race was 135 ± 8 (range 124–147) bpm. Race completion led to a small and non-significant reduction in BM (71.9 ± 11.3 to 71.0 ± 11.0 kg, P > 0.05). Data for a range of indices related to LV preload were not significantly altered. Specifically, LV end-diastolic area (20.2 ± 3.0 to 19.7 ± 2.5 cm2, P > 0.05) and volume (102 ± 20 to 95 ± 21 mL, P > 0.05) and left atrial diameter (3.8 ± 0.4 to 3.8 ± 0.4 cm, P > 0.05) were not significantly different post-race. Left ventricular meridional wall stress (41.3 ± 4.0 to 37.2 ± 2.1 dynescm3, P < 0.05), an index of afterload, was significantly reduced post-race. Heart rate was significantly increased post-race (60 ± 8 to 79 ± 9 bpm, P < 0.05).
Ejection fraction, fractional area change, and the end-systolic pressure–volume ratio were significantly reduced post-race (Table 1). Global indices of LV diastolic filling: E and E/A were significantly reduced (P < 0.05), E deceleration time was significantly lengthened (P < 0.05) whereas A was not changed post-race (P > 0.05; Table 1).
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Segmental and mean data for strain and strain rate are presented in Figures 1–3. In the circumferential plane, peak strain and peak E strain rate were significantly reduced in all segments (P < 0.05; Figure 1). Peak S strain rate was reduced in some (lateral, anterior, and posterior) segments as well as in the calculated mean score (P < 0.05). In the radial plane, peak strain was significantly reduced post-race in all segments (except septal, Figure 2). Peak S strain rate was not significantly reduced in any segment (P > 0.05). In all segments, except septal and inferior, peak E strain rates were significantly reduced post-race. As a consequence, mean peak E strain rate was also significantly reduced (P < 0.05). In the longitudinal plane, septal, lateral, and mean peak strain were significantly reduced (P < 0.05; Figure 3). This was mirrored by a reduction in septal and lateral peak S strain rate (P < 0.05). Despite a trend for a reduction in peak E strain rates, these were not significantly different in all segments or in the mean score (P > 0.05). Correlational analyses of changes in strain and strain rate data with age, finishing time, as well as differences (delta) in indices of preload, afterload, and heart rate produced low (maximum r2 = 0.22) and non-significant relationships (P > 0.05).
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) as well as systolic (S) and early diastolic (E) strain rate data for the circumferential plane pre- and post-race.
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Qualitative analysis of individual peak strain data identified three runners with segment-specific responses to exercise. Specifically, one individual had markedly reduced radial and circumferential peak strain in septal and anteroseptal segments with little or no change in peak strain in other wall segments (Figure 4). A further subject had a marked reduction in peak radial strain in the septal wall segment and one subject had decreased radial and circumferential peak strain in the anterior and lateral wall segments.
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Serum cTnT was undetectable in all 12 athletes prior to the race. After the race, 5/12 (42%) athletes presented with a cTnT above the assay detection limit (0.01 µg/L) with a range of 0.013–0.272 µg/L. The comparison of mean strain and strain rate data between subjects with and without a post-race elevation in cTnT did not reveal any significant differences (t = 0.298–0.954, P > 0.05). Of the runners with segmental-specific responses to exercise, one did and one did not have detectable troponin post-exercise. The third athlete did not provide a post-race blood sample.
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Myocardial speckle tracking data for peak strain, peak systolic strain rate, and early diastolic strain rate collected after an ultra-marathon run of 89 km provided evidence of a depression in LV function post-race. Of interest, however, was individual evidence of heterogeneous patterns of segmental peak strain and strain rate data after race completion. The appearance of cTnT in the systemic circulation was also noted in 5 runners.
A depression in indices of global systolic and diastolic function recorded after the Comrades Marathon is similar to a recent multi-event ultra-distance study.1 This gives some support to a duration-dependent effect for post-exercise changes in LV function.2,20 The ‘picture’ of depression in cardiac function after prolonged exercise provided by global indices is somewhat limited due to the lack of sensitivity to changes in cardiac motion that may occur in different planes as well as in a range of wall segments. Thus, the value of speckle tracking-derived peak strain and strain rate data, over global indices or tissue Doppler data, is provided by interrogation of segmental LV motion. In both radial and circumferential planes, peak strain was significantly reduced in most segments. The reduction in peak strain suggests that maximal LV wall deformation is reduced post-exercise (although the rate of deformation is less affected) and this supports changes in global indices of contractility.1 The reduction in peak early diastolic strain rate also supports global changes in diastolic filling suggesting that the rate of ventricular relaxation is impaired.3 Data from longitudinal scans were less consistent with only sporadic segmental evidence of change in strain or strain rate post-exercise. Owing to the relatively small, longitudinally aligned, sub-endocardial myocyte mass, it has often been reported that the ejection phase motion more closely reflects circumferential fibre shortening in the short axis.21 Of specific future interest may be the differentiation in the response to exercise of peak strain/strain rate data derived from sub-endocardial and sub-epicardial portions of the myocardium. Currently, the ability to analyse these areas separately is not afforded by the scanning systems.
The underlying mechanism(s) for explaining altered strain and strain rate after prolonged exercise cannot be determined directly from this study. Concern has been expressed that changes in LV function simply represent the impact of reduce LV preload, augmented afterload, and/or a raised HR often reported after prolonged exercise. Indeed, we cannot directly discount these factors but would make the following observations. In the current study, changes in estimates of preload were non-significant. Despite this, we correlated change scores for preload with changes scores for systolic and diastolic function and these were also non-significant, suggesting that the magnitude of change in preload could not explain a significant proportion of the variance in LV functional indices. Changes in LV function in the face of limited alterations in preload, as well as small correlations between delta scores, have been reported previously in a laboratory-based study.22 Indices of afterload were actually reduced post-race so this unlikely to explain a reduction in LV function. The elevated HR post-race did not explain a significant portion of the variance in LV function change via correlational analysis of change scores. Interestingly, when HR is increased to levels similar to those observed in the current study, Doppler and tissue Doppler data for early and atrial filling and tissue velocities actually increase,23 which again is at odds with the current data. Further in a laboratory study where HR was matched pre- and post-prolonged exercise evidence of changes in systolic and diastolic function persisted.22 Finally, global changes in preload, afterload, or HR could not explain the heterogeneous peak strain data observed in different LV wall segments from the same two-dimensional short-axis scans (Figure 4). Other potential mechanisms are worth some brief speculative comment. Recent research has highlighted a potential role for β-adrenergic desensitization after prolonged exercise likely as a consequence of chronically elevated catecholamines during ultra-endurance exercise.22,24,25 This may partially explain the global decline in LV systolic function observed in some individuals but, again, would unlikely explain segmental-specific changes. Further, β-adrenergic desensitization has not explained changes in diastolic function after prolonged exercise.22 The potential impact of myocyte damage or injury on LV function was assessed via cTnT. Although cTnT rose post-race in 42% of runners, which is similar to data from conventional marathons,4,7 the presence of cTnT in the systemic circulation post-race was not related to changes in LV function. Although this lack of association has been challenged by Rifai et al.,12 it confirms other data previously published6,7 and suggests that after prolonged exercise a decline in LV function in well-trained athletes is at least partially due to mechanisms other than reversible tissue damage. The mechanism(s) behind both exercise-related changes in LV function and elevations in cTnT remain to be elucidated. The time-course and magnitude of cTnT release has prompted suggestions that it has its origin in the cytosol and may reflect a free radical-mediated transient increase in cell membrane permeability.26
Of specific interest within the current study was the demonstration of a heterogeneous individual and segmental response to prolonged exercise (see exemplar Figure 4). The subject in Figure 4, and one other subject, demonstrated a marked reduction in peak radial strain primarily in the septal and anteroseptal segments. A further subject had reduced radial and circumferential strain in anterior and lateral segments. The segmental changes in the septum correspond to previous data from standard two-dimensional scans scored semi-quantitatively, after an Ironman triathlon.11,12 Douglas et al.11 documented a depression in septal regional chord shortening/area ejection fraction in the septal wall and Rifai et al.12 reported, semi-quantitatively, reduced anterospetal and apical wall motion. Such regional changes in LV function are also supported by evidence of abnormal thallium uptake in the septum of runners after treadmill running.27 Interestingly, an increase in abnormal wall motion score was associated with higher serum troponin concentrations post-race12 which is not supported by the current data (one subject had an elevated cTnT post-race; the other did not, with the third athlete not providing a sample). As was hypothesized by Douglas et al.,11 a reduction in function in septal and anteroseptal segments post-race may suggest a role for ventricular interaction and/or right ventricular dysfunction. Alternatively, the current data may tie in with previous reports of pulmonary oedema in two competitors completing the Comrades Marathon in the 1970s.13 We did not collect right ventricular dimension, function, strain, or strain rate data which may have illuminated these issues. Other mechanisms to explain regional changes (either septal, anterior, and/or lateral wall) in function are also speculative but may include regional abnormalities in blood flow, ischaemia, and/or metabolism. Further work is required to fully understand individual and segmental differences in the response of LV function to prolonged exercise.
As with any field study, some limitations prompt on-going study. Specifically, we have reported strain and strain rate data for basal wall segments only and further research assessing 16 wall segments including mid and apical wall motion would provide a more comprehensive picture of LV function as well as facilitating the assessment of rotation, rotation rates, and torsion.28 It is of course pertinent to detail the limitations of myocardial speckle tracking. The technique is highly dependent on image quality; validation studies of radial and circumferential strain are on-going and clinical applications are still under development. A relative lack of normal data limits our ability to interpret segmental heterogeneity as well as pre–post-exercise changes; however, previous data from tissue-Doppler-derived strain suggests longitudinal strains are homogenously distributed. Further, on-going development of speckle track technology may allow interrogation of strain and strain rate in sub-endocardial vs. sub-epicardial segments of the myocardium. We did not obtain any follow-up data, although LV changes have been reported previously to be transient with a return to baseline within 48 h,29 although recent data have questioned this9 and clarification is required. Finally, we collected no formal record of clinical signs and symptoms in this cohort, but all were conscious, responsive, and were able to self-ambulate after the post-race assessment.
In conclusion, completion of the Comrades Marathon resulted in changes in indices of LV systolic and diastolic function. Global and segmental two-dimensional strain data were affected, although there was heterogeneity in response between individuals as well as between LV wall segments and planes of motion. Age, finishing time, and LV loading changes with the race did not mediate these effects. Five runners presented with post-race cTnT above the assay detection limit, but these were unrelated to any changes in LV function. Future research should attempt to determine the reasons for individual specific responses in LV function and cardiac biomarker release that occurs consequent to ultra-endurance exercise.
Conflict of interest: none declared.
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Work in the MRC/UCT Research Unit for Exercise Science and Sports Medicine, University of Cape Town, is supported by the University, the Medical Research Council and Discovery Health.
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We are grateful to Jason Worthy and Sheena Privett, our subjects, the organizers and Medical team at the Comrades Marathon, and colleagues from the University of Cape Town who helped facilitate this work. We thank GE UK and GE SA for providing technical assistance.
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