Persistent and reversible cardiac dysfunction among amateur marathon runners

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1 European Heart Journal (2006) 27, doi: /eurheartj/ehi813 Clinical research Heart failure Persistent and reversible cardiac dysfunction among amateur marathon runners Tomas G. Neilan 1, Danita M. Yoerger 1, Pamela S. Douglas 4, Jane E. Marshall 1, Elkan F. Halpern 3, David Lawlor 2, Michael H. Picard 1, and Malissa J. Wood 1 * 1 Cardiac Ultrasound Laboratory, Division of Cardiology, Department of Medicine, Massachusetts General Hospital and Harvard Medical School, 55 Fruit Street, VBK 508, Boston, MA , USA; 2 Division of Pediatric Surgery, Department of Surgery, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA; 3 Institute for Technology Assessment, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA; and 4 Division of Cardiology, Duke University Medical Center, Durham, NC, USA Received 24 May 2005; revised 2 February 2006; accepted 9 February 2006; online publish-ahead-of-print 22 March 2006 KEYWORDS Endurance sport; Diastolic dysfunction; Tissue Doppler Aims Transient systolic and diastolic abnormalities in ventricular function have previously been documented during endurance sports. However, these described alterations may be limited by the techniques applied. We sought, using less load-dependent methods, to characterize both the extent and the chronology of the cardiac changes associated with endurance events. Methods and results Transthoracic echocardiography (TTE) was performed prior to, immediately after, and approximately 1 month after completion of the 2003 Boston Marathon in 20 amateur athletes. TTE included two-dimensional, spectral and tissue Doppler (TD) and flow propagation velocity (V p ). After completion of the marathon, global measures of left ventricular (LV) systolic function were unchanged (EF 59+6 vs % post, P ¼ 0.14), whereas TD-derived measures of LV systolic function [septal strain vs %, P ¼ 0.007; septal strain rate (SR) vs s 21, P ¼ 0.007] and right ventricular (RV) systolic function (RV apical strain vs %, P ¼ 0.001; RV apical SR vs , P ¼ 0.002) were reduced. Significant changes in transmitral velocity (E/A ratio vs , P ¼ 0.005) and TD indices of LV and RV diastolic function (E a septal vs cm/s post-marathon, P ¼ 0.01) were also observed, indicating an inherent alteration in LV relaxation. Although all indices of LV and RV systolic function had returned to normal on follow-up, there were persistent diastolic abnormalities (RV E a, cm/s pre-marathon vs cm/s follow-up, P ¼ 0.01). Conclusion Marathon running leads to transient systolic and more persistent diastolic dysfunction of both the LV and the RV. Introduction Participation in endurance sports has increased in the past decade; in the USA alone, nearly runners completed a marathon in Although the cardiovascular benefits of moderate exercise are well established, 1 cardiovascular effects of prolonged exertion are less clear. While the risk of sudden death associated with participation is small: 2 participation in such events is consistently associated with biochemical evidence of cardiac damage and dysfunction. 3 Previous echocardiographic studies have suggested that cardiac dysfunction or cardiac fatigue occurs during prolonged exercise. 4 These studies have documented minimal decreases in global left ventricular (LV) systolic function, alterations in LV diastolic function, and the appearance of wall * Corresponding author. Tel: þ ; fax: þ address: mjwood@partners.org motion abnormalities. 5,6 These studies may be limited by the contribution of alterations in loading conditions. Also, apart from the extent, the chronology of these changes is unclear. Less load-dependent echocardiographic techniques are now available, which can be used to quantify regional and global systolic and diastolic function with greater accuracy. These techniques include pulsed-tissue Doppler (TD), 7 strain and strain rate (SR) imaging. 8 Therefore, we aimed to characterize the extent and the chronology of the cardiac changes associated with endurance sports using both load-dependent and load-independent techniques among amateur participants. Methods Experimental protocol The investigational protocol was approved by the Partners Healthcare System Human Subjects Review Committee and The Boston Athletic Association. All subjects gave written informed & The European Society of Cardiology All rights reserved. For Permissions, please journals.permissions@oxfordjournals.org

2 1080 T.G. Neilan et al. consent before participation. Because of the extensive resource requirements, the initial study group was limited to 30 amateur runners registered for the 2003 Boston marathon and recruited from local running clubs by open invitation. Final exclusion criteria included cardiovascular disease and age,18 or.55 years. Echocardiography was performed within 1 week prior to the marathon, immediately after the athlete crossed the finish line, and at follow-up, between 3 4 weeks after the marathon. Blood pressure, heart rate, and weight were measured prior to each echocardiographic study. Echocardiographic studies Conventional echocardiography The studies were performed using a commercially available echocardiography machine equipped with a 2.5 MHz probe and digital storage capacity (General Electric Vivid 7, Milwaukee, WI, USA). A complete echocardiographic study was performed in twodimensional and TD modes. Three cardiac cycles of each view were collected and stored. All TD images were obtained at a frame rate of at least 100 frames per second. Two-dimensional measurements included LV end-diastolic and end-systolic volumes (biplane Simpson s rule), right ventricular (RV) areas and LV mass (truncated ellipsoid method). Pulsed Doppler imaging was used to interrogate transmitral, pulmonary venous, and LV outflow tract flow. The mitral inflow E and A-wave velocities, pulmonary systolic (S), and diastolic (D) velocities were measured. From these, the E/A and S/D ratios were calculated. The aortic ejection time was calculated from the pulsed Doppler tracing in the apical five-chamber view. Three beats were measured and the average reported for all Doppler echocardiographic variables. Flow propagation velocity (V p ) Colour M-mode flow propagation velocity was acquired from apical four-chamber view with the cursor placed through mitral leaflet tips in parallel with mitral inflow and extending 4 cm into the LV cavity. A clear first aliasing velocity was produced by shifting the colour baseline upward. TD measurements The imaging angle was adjusted to ensure a parallel alignment of the beam with the myocardial segment of interest and thus minimize the angle dependency for all Doppler tracings. For pulsed TD measurement of the mitral annular velocities [early (E a )andlate (A a )], the sample volume ( pixels) was placed at the septal and lateral mitral annulus. Tricuspid annular velocities were measured with the sample volume placed in the lateral annulus. Colour TD measurements of LV myocardial function were performed in the apical four-chamber view. 9 For peak LV systolic strain and SR images, the sample volume was placed in the mid-septum and lateral ventricular wall. Peak strain and SR were defined as the greatest value on the strain curve. Similarly, for peak RV strain and SR, analysis was performed with the sample volume placed at the basal (tricuspid annulus), mid and apical (RV free wall at the moderator band) levels in the apical four-chamber view. The position of the sample volume was manually adjusted frame by frame throughout the cardiac cycle to ensure its position within the myocardium. Strain length of 12 mm was used to compute the strain and SR. All measurements were taken from three beats and averaged. Regional analysis of myocardial wall velocities, strain, and SR was performed offline using computer software (EchoPac, Version 6.3, General Electric). Observer variability Interobserver variability was calculated as the SD of the differences in measurements by two independent observers for 30 randomly selected tracings of annular TD, strain, and SR. These were equally distributed between baseline, post-marathon, and follow-up echocardiographic studies. Statistics Data are presented as mean + SD. Repeated analysis of variance was used to compare the changes in echocardiographic parameters. In the analysis, the only term was time, no grouping factors were used and the only effect of interest was the changes in echo-derived variables over time. All tests were two-sided where appropriate. We controlled for multiple comparisons by performing pair-wise comparisons only if the overall P-value for time was significantly different. Significance was set at a P, Results All responders between the age brackets specified were initially included and no subject refused consent. Only patients with complete pre-, post-, and follow-up echoes were included in the initial analysis (22 of the initial 30 subjects). We excluded those who, due to scheduling difficulties, were unable to attend for follow-up imaging. Two subjects were also excluded from final analysis due to persistent hypertension. Therefore, there were a total of 20 subjects available for analysis. These included 10 males and 10 females with a mean age of years, marathon finish time of h and LV mass of g/m 2. The chamber dimensions, volumes, and function at rest for this cohort were within normal limits. Body weight decreased from to kg after the marathon. Diastolic blood pressure remained unchanged, whereas there was a reduction in systolic pressure (Table 1) and an increase in the heart rate following the marathon ( baseline vs bpm postmarathon, P ¼ ). These parameters had returned to normal at follow-up. Conventional echocardiography No significant post-marathon changes were observed in either LV dimensions or volumes or RV dimensions or area on completion of the marathon (Table 1). The LV ejection fraction (LVEF) and the percentage RV area were also unchanged. The left atrial dimension decreased significantly following the marathon (from baseline to cm post-marathon, P ¼ 0.004). The peak transmitral E-wave velocity decreased, while the transmitral A-wave increased (41+8 baseline vs cm/s post-marathon, P ¼ 0.004) (Table 2). These changes yielded a significant decrease in the E/A ratio ( baseline vs post-marathon, P ¼ 0.005) from pre- to post-marathon. Pulmonary venous S and D-wave velocities remained unchanged. The transmitral A-wave velocity and the E/A ratio remained abnormal on follow-up. Pulsed-TD Similar to the transmitral filling pattern, early annular velocities also decreased significantly (E a septal baseline vs cm/s post-marathon, P ¼ 0.01) (Table 3), whereas late diastolic annular velocities (A a ) increased after completion of a marathon ( baseline vs cm/s post-marathon, P ¼ 0.02). The E/E a ratio

3 Cardiac dysfunction among amateur marathon runners 1081 Table 1 Haemodynamic and two-dimensional echo data Weight (kg) HR (bpm) SBP (mmhg) DBP (mmhg) LA (cm) LVEDD (cm) LVESD (cm) LVEDV (ml) LVESV (ml) RVDD (mm) RVAS (cm 2 ) RVAD (cm 2 ) LVEF (%) RV area D HR, heart rate; SBP, systolic blood pressure; DBP, diastolic blood pressure; LA, left atrial anterior-posterior dimensions; LVEDD, left ventricular end-diastolic dimensions; LVESD, left ventricular end-systolic dimensions; LVEDV, left ventricular end-diastolic volume; LVESV, left ventricular end-systolic volume; RVDD, right ventricular diastolic dimensions; RVAS, right ventricular area in systole; RVAD, right ventricular area in diastole; LVEF, left ventricular ejection fraction; RV area D, change in RV area from diastole to systole. Table 2 Transmitral, transpulmonary, and aortic Doppler indices E (cm/s) A (cm/s) E/A PV S (cm/s) PV D (cm/s) PV S/D ET (ms) E, peak transmitral E-wave velocity; A, peak transmitral A-wave velocity; E/A, ratio of transmitral E to transmitral A; PV S, peak pulmonary vein systolic flow velocity; PV D, peak pulmonary vein diastolic flow velocity; PV S/D, ratio of pulmonary vein systolic to diastolic flow; ET, aortic ejection time. Table 3 Pulsed TD and M-mode indices of diastolic function E a septal (cm/s) E a lateral (cm/s) A a septal (cm/s) A a lateral (cm/s) V p (cm/s) E/E a (lateral) E a, early diastolic annular velocity measured in the both the septal and lateral annulus; A a, late diastolic annular velocity measured in both the septal and lateral annulus; V p, mitral inflow flow propagation velocity; E/E a, ratio of peak early transmitral diastolic velocity to early lateral annular velocity. remained in the normal range ( vs , P ¼ 0.63). Consistent with the reduction in annular TD E a, the flow propagation velocity (V p ) also decreased following the marathon (55+5 baseline vs cm/s post-marathon, P ¼ 0.01). Early and late annular velocities of both the LV and RV remained abnormal on follow-up (E a lateral baseline vs cm/s follow-up, P ¼ 0.008) (Tables 3 and 5).

4 1082 T.G. Neilan et al. LV strain and SR Although conventional indices of LV systolic function remained unchanged, both peak systolic strain and SR in the septal and lateral wall decreased. Significant post-marathon decreases were observed in peak LV systolic strain (Table 4) in both the septal (223+5 baseline vs % post-marathon, P ¼ 0.007) and lateral territories (221+6 baseline vs % post-marathon, P ¼ 0.007) (Figure 1). Peak septal and lateral SR also decreased post-marathon (septal SR baseline vs s 21 post-marathon, P ¼ 0.007). These abnormalities of LV systolic function had normalized on follow-up. RV strain and SR At rest, there was a gradient in peak systolic strain and SR from the base to the apex of the RV (Table 5). When compared with the pre-marathon values, apical RV strain and SR decreased (233+4 baseline vs % post-marathon, P ¼ and baseline vs postmarathon, P ¼ 0.002, respectively); these returned to baseline on follow-up. Interobserver variability Interobserver variability for annular TD was 4.3%, P ¼ 0.78, for strain 7%, P ¼ 0.59, and for SR was 4.5%, P ¼ Discussion We followed non-competitive athletes participating in the 2003 Boston marathon using serial echocardiography and demonstrated attenuation of systolic and diastolic myocardial function. Prolonged exercise is associated with alterations in loading conditions; this may limit the ability of traditional cardiac indices to detect dysfunction. However, using less load-dependent techniques, we found that participation in this event was also associated with Table 4 TD strain, and SR indices of LV systolic function TD Sys (septum) (cm/s) TD Sys (lateral) (cm/s) SR (septal) (s 21 ) SR (lateral) (s 21 ) Strain (septal) (%) Strain (lateral) (%) TD Sys, peak myocardial systolic endocardial velocities in the septum and lateral walls; SR, peak systolic strain rate measured in the septal and lateral walls; strain, peak systolic strain measured in the septal and lateral walls. Figure 1 Left ventricular septal longitudinal strain pre- and post-marathon in a 28-year-old female participant.

5 Cardiac dysfunction among amateur marathon runners 1083 Table 5 RV TD analysis Ea (cm/s) Aa (cm/s) Strain base (%) Strain mid (%) Strain apex (%) SR base (s 21 ) SR mid (s 21 ) SR apex (s 21 ) Ea, early diastolic annular velocity measured in the lateral tricuspid annulus; Aa, late diastolic annular velocity measured in lateral tricuspid annulus; strain, measured at the base, mid, and apex of the right ventricle; SR, strain rate measured at the base, mid, and apex of the right ventricle. changes in indices of LV and RV systolic and diastolic functions. We also demonstrate that although all of the systolic abnormalities had normalized, diastolic abnormalities of the LV and RV persisted up to 1 month after participation. Doppler examination of mitral inflow has been widely used to evaluate LV diastolic function. However, it is affected by several factors including LA pressure and volume status. 10 Pre-load may be altered during marathon running by dehydration, redistribution of blood flow, and increased HR, whereas afterload may be affected by changes in blood pressure. Mitral annular velocities have been reported to be a relatively load-independent index of LV relaxation, 11 and E/E a has been shown to be an accurate predictor of LA pressure. 12 Septal annular velocities may be subjected to the influence of the RV, whereas lateral velocities may be affected by both translational effects 13 and beam angle. 14 We recorded annular velocities in both walls and found consistent changes in both the septal and lateral walls reflecting attenuation of early diastolic filling and augmentation of late filling. If this reduction in early diastolic filling was a response to altered loading conditions, one would also expect to see a similar decrease in the late diastolic filling. 15 This suggests that the cardiac response to participation in such events is associated with an intrinsic shift in LV filling. Although elevation of E/E a is a marker of increased LA pressure, 16 in our cohort E/E a was normal and remained unchanged despite weight loss and decreased LA size. This supports previous observations that this Doppler index may not be sensitive for detecting decreases in ventricular end-diastolic pressure, especially within the normal range. 17 Echocardiographic strain and SR imaging allows noninvasive and less load-dependent assessment of myocardial function. 18 We measured peak longitudinal SR, which has been shown to closely correlate with invasive markers of LV contractility, such as dp/dt Max, and because it is less susceptible to translation and tethering artefacts, it is more accurate than annular velocities in assessing regional myocardial dysfunction. 9,19 Although traditional markers of LV systolic function remained unchanged, we found that both strain and SR decreased significantly from pre- to postmarathon. Previous studies have documented global myocardial systolic dysfunction during more prolonged endurance events. 4 This systolic dysfunction detected returned to normal within 48 h of the event. 5 The absence of change in global LV function in our study is similar to that reported elsewhere 20 and may be related to the duration of exercise. Also, similar to previous work in other models, 9 this suggests that TD may detect sub-clinical dysfunction prior to alterations in global measures such as ejection fraction. Similar to the LV, changes in systolic and diastolic RV function occurred with exercise; the diastolic changes mirrored those seen in the LV. Despite an increase in heart rate, 21 there was a trend towards reduction in RV strain in all segments studied; this reached statistical significance in the apex, suggesting that when assessing RV contractility the distal free wall may provide the most accurate representation of function. There are disadvantages of TD imaging and these include decreased signal-to-noise ratio (particularly with SR) and the angle dependency of the signal. 22 In contrast, these measures are not dependent on boundary detection for quantification of contractile function and the intraobserver and interobserver variability is usually,15%. 23 Follow-up studies were performed to assess the chronology of the cardiac changes. Similar to our observations, other groups have noted immediate recovery of global systolic function. 24 However, in our cohort of average athletes, some of the diastolic abnormalities persisted, and these affected both the LV and the RV. Although the significance of prolonged diastolic abnormalities in other models of ventricular dysfunction is clear, 25 its implications in our cohort is uncertain. In elite athletes with LV hypertrophy, the majority of whom were not runners, it has been previously shown that de-training is associated with a reduction in early diastolic filling, an increase in transmitral A-velocities, and a consequent reduction in the E/A ratio. 26,27 Similarly, even though our athletes had normal cavity dimensions and mass, we found similar changes in diastolic filling. This suggests that the de-training phenomenon is similar regardless of the athletic substrate and also suggests that the diastolic changes associated with deconditioning occur earlier rather than later. However, it is still unclear whether these diastolic changes are part of normal recovery from a period of intense training, whether they truly represent a period of persistent diastolic dysfunction after an endurance event, and whether there are any associated long-term cardiac sequelae. Our study has several possible limitations. We have alluded to most of the limitations related to the echocardiographic techniques previously. The study group is small and we are not able to comment on possible gender differences in the

6 1084 T.G. Neilan et al. cardiac response to endurance sports. Our results do not pertain to elite athletes; our group consisted of runners who ran on average less than 40 miles a week during training, a level that is most consistent with the average marathon runner. Also our study does not address whether this transient dysfunction leads to cardiac damage or whether there are any long-term cardiac sequelae to repetitive marathon running. As discussed previously, most non-invasive indices of LV performance are significantly influenced by changes in the loading conditions associated with participation in a marathon. Although we selected indices that are least affected by load, animal studies have suggested that in normal hearts even these TD indices may not be completely independent of load. 15,28 Liberal use of isotonic fluid replacement was encouraged throughout the run and immediately on crossing the finish line in an attempt to minimize significant volume depletion. This is reflected in the minimal changes in LV size, blood pressure, and weight at the finish line. LV strain and SR were measured in the mid-septal and lateral walls. We chose to measure strain in these regions due to optimal ultrasound beam alignment, the previously noted problems with annular motion at the base and the unreliability of apical LV strain quantification. We also did not measure radial strain as longitudinal strain appears to be subject to less variability. 8,19 This study was designed with the intent of further characterizing and quantifying the cardiac changes which occur during participation in prolonged vigorous physical activity. Athletes demonstrated transient systolic abnormalities and more prolonged diastolic abnormalities. Acknowledgements We would like to acknowledge the assistance of Marvin Adner, MD medical director of the Boston Athletic Association for his contribution to the initiation and progression of this study. We would also like to thank Genevieve Derumeaux, MD for her expert guidance. Lastly, we would like to acknowledge GE Healthcare for their equipment loan and technical support. T.G.N. is supported by an Irish Board for Training in Cardiovascular Medicine and Department of Health and Children Cardiovascular Health Strategy Traveling Fellowship and an American Society of Echocardiography Research Fellowship award. Conflict of Interest: none declared. References 1. Sandvik L, Erikssen J, Thaulow E, Erikssen G, Mundal R, Rodahl K. Physical fitness as a predictor of mortality among healthy, middle-aged Norwegian men. N Engl J Med 1993;328: Maron BJ, Shirani J, Poliac LC, Mathenge R, Roberts WC, Mueller FO. Sudden death in young competitive athletes. Clinical, demographic, and pathological profiles. JAMA 1996;276: Siegel AJ, Silverman LM, Evans WJ. Elevated skeletal muscle creatine kinase MB isoenzyme levels in marathon runners. JAMA 1983;250: Douglas PS, O Toole ML, Hiller WD, Hackney K, Reichek N. Cardiac fatigue after prolonged exercise. Circulation 1987;76: Douglas PS, O Toole ML, Woolard J. Regional wall motion abnormalities after prolonged exercise in the normal left ventricle. Circulation 1990; 82: Perrault H, Peronnet F, Lebeau R, Nadeau RA. Echocardiographic assessment of left ventricular performance before and after marathon running. Am Heart J 1986;112: McMahon CJ, Nagueh SF, Pignatelli RH, Denfield SW, Dreyer WJ, Price JF, Clunie S, Bezold LI, Hays AL, Towbin JA, Eidem BW. Characterization of left ventricular diastolic function by tissue Doppler imaging and clinical status in children with hypertrophic cardiomyopathy. Circulation 2004; 109: D Hooge J, Herbots L, Sutherland GR. Quantitative assessment of intrinsic regional myocardial deformation by Doppler strain rate echocardiography in humans. Circulation 2003;107:e49; author reply e Wong CY, O Moore-Sullivan T, Leano R, Byrne N, Beller E, Marwick TH. Alterations of left ventricular myocardial characteristics associated with obesity. Circulation 2004;110: Choong CY, Herrmann HC, Weyman AE, Fifer MA. Preload dependence of Doppler-derived indexes of left ventricular diastolic function in humans. J Am Coll Cardiol 1987;10: Nagueh SF, Middleton KJ, Kopelen HA, Zoghbi WA, Quinones MA. Doppler tissue imaging: a noninvasive technique for evaluation of left ventricular relaxation and estimation of filling pressures. J Am Coll Cardiol 1997; 30: Nagueh SF, Lakkis NM, Middleton KJ, Spencer WH III, Zoghbi WA, Quinones MA. Doppler estimation of left ventricular filling pressures in patients with hypertrophic cardiomyopathy. Circulation 1999;99: Heimdal A, Stoylen A, Torp H, Skjaerpe T. Real-time strain rate imaging of the left ventricle by ultrasound. J Am Soc Echocardiogr 1998; 11: Sohn DW, Chai IH, Lee DJ, Kim HC, Kim HS, Oh BH, Lee MM, Park YB, Choi YS, Seo JD, Lee YW. Assessment of mitral annulus velocity by Doppler tissue imaging in the evaluation of left ventricular diastolic function. J Am Coll Cardiol 1997;30: Jacques DC, Pinsky MR, Severyn D, Gorcsan J III. Influence of alterations in loading on mitral annular velocity by tissue Doppler echocardiography and its associated ability to predict filling pressures. Chest 2004; 126: Dokainish H, Zoghbi WA, Lakkis NM, Al-Bakshy F, Dhir M, Quinones MA, Nagueh SF. Optimal noninvasive assessment of left ventricular filling pressures: a comparison of tissue Doppler echocardiography and B-type natriuretic peptide in patients with pulmonary artery catheters. Circulation 2004;109: Ommen SR, Nishimura RA, Appleton CP, Miller FA, Oh JK, Redfield MM, Tajik AJ. Clinical utility of Doppler echocardiography and tissue Doppler imaging in the estimation of left ventricular filling pressures: a comparative simultaneous Doppler-catheterization study. Circulation 2000;102: Smiseth OA, Ihlen H. Strain rate imaging: why do we need it? J Am Coll Cardiol 2003;42: Greenberg NL, Firstenberg MS, Castro PL, Main M, Travaglini A, Odabashian JA, Drinko JK, Rodriguez LL, Thomas JD, Garcia MJ. Dopplerderived myocardial systolic strain rate is a strong index of left ventricular contractility. Circulation 2002;105: Whyte G, George K, Shave R, Dawson E, Stephenson C, Edwards B, Gaze D, Oxborough D, Forster J, Simspon R. Impact of marathon running on cardiac structure and function in recreational runners. Clin Sci (Lond) 2005;108: Jamal F, Strotmann J, Weidemann F, Kukulski T, D Hooge J, Bijnens B, Van de Werf F, De Scheerder I, Sutherland GR. Noninvasive quantification of the contractile reserve of stunned myocardium by ultrasonic strain rate and strain. Circulation 2001;104: Pislaru C, Abraham TP, Belohlavek M. Strain and strain rate echocardiography. Curr Opin Cardiol 2002;17: Edvardsen T, Skulstad H, Aakhus S, Urheim S, Ihlen H. Regional myocardial systolic function during acute myocardial ischemia assessed by strain Doppler echocardiography. J Am Coll Cardiol 2001;37: Douglas PS, O Toole ML, Hiller WD, Reichek N. Different effects of prolonged exercise on the right and left ventricles. J Am Coll Cardiol 1990;15: Nijland F, Kamp O, Karreman AJ, van Eenige MJ, Visser CA. Prognostic implications of restrictive left ventricular filling in acute myocardial infarction: a serial Doppler echocardiographic study. J Am Coll Cardiol 1997;30: Pelliccia A, Maron BJ, De Luca R, Di Paolo FM, Spataro A, Culasso F. Remodeling of left ventricular hypertrophy in elite athletes after long-term deconditioning. Circulation 2002;105: Naylor LH, Arnolda LF, Deague JA, Playford D, Maurogiovanni A, O Driscoll G, Green DJ. Reduced ventricular flow propagation velocity in elite athletes is augmented with the resumption of exercise training. J Physiol 2005;563: Firstenberg MS, Greenberg NL, Main ML, Drinko JK, Odabashian JA, Thomas JD, Garcia MJ. Determinants of diastolic myocardial tissue Doppler velocities: influences of relaxation and preload. J Appl Physiol 2001;90:

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