The Role of Three-Dimensional Echocardiography in the Assessment of Right Ventricular Dysfunction after a Half Marathon: Comparison with Cardiac Magnetic Resonance Imaging




Background


Although marathon running is associated with transient right ventricular (RV) systolic dysfunction as detected by two-dimensional transthoracic echocardiography, quantitative assessment of the right ventricle is difficult because of its complex geometry. Little is known about the use of real-time three-dimensional echocardiography (RT3DE) in the detection of cardiac dysfunction after a half marathon. The aim of this study was to assess the extent of RV dysfunction after the completion of a half marathon using cardiac biomarkers, RT3DE, and cardiac magnetic resonance imaging (CMR).


Methods


A prospective study was performed in 15 individuals in 2009 participating in the Manitoba Half Marathon. Cardiac biomarkers (myoglobin, creatine kinase–MB and cardiac troponin T) were assessed and RT3DE and CMR were performed 1 week before, immediately after, and 1 week after the race.


Results


At baseline, cardiac biomarkers and ventricular function were within normal limits. Immediately following the half marathon, all patients demonstrated elevated cardiac troponin T levels, with a median value of 0.37 ng/mL. RV ejection fraction, as assessed by RT3DE, decreased from 59 ± 4% at baseline to 45 ± 5% immediately following the race ( P < .05). On CMR, RV end-diastolic volume increased after the half marathon, and the RV ejection fraction was reduced, at 47 ± 5% compared with 60 ± 2% at baseline ( P < .05). There were strong linear correlations between RV ejection fraction assessed by RT3DE and CMR at baseline and after the half marathon ( r = 0.69 and r = 0.87, P < .01, respectively).


Conclusions


Compared with CMR, RT3DE is a feasible and reproducible method of assessing transient RV dysfunction in athletes completing a half marathon.


Marathon running has become increasingly more popular over the past decade, for both amateur and elite athletes. Research into the short-term consequences of endurance exercise on cardiac function, especially the right ventricle, has recently increased. Previous studies have found that the elevation of cardiac biomarkers in marathon runners, in particular myoglobin, creatine kinase (CK), and cardiac troponin T (cTnT), correlate with transient changes in right ventricular (RV) function as assessed by echocardiography. Although multiple studies have demonstrated two-dimensional echocardiographic evidence of transient RV systolic and diastolic abnormalities after endurance sports, quantitative assessment of the right ventricle is difficult because of its complex geometry.


The recent introduction of real-time three-dimensional echocardiography (RT3DE) has shown to be a feasible and reliable method of assessing RV ejection fraction (RVEF). A number of studies have compared RT3DE to cardiac magnetic resonance imaging (CMR) in the assessment of RV volumes and RVEF, demonstrating a high correlation with excellent intraobserver and interobserver reliability. As a result, RT3DE has proven to be a cost-effective, a less invasive, and an accurate means of assessing RV function in a variety of cardiac disorders. Little is known, however, about the utility of RT3DE in the noninvasive assessment of the right ventricle after a marathon.


Recently, CMR has been used to validate RV systolic dysfunction following a full marathon. Similar to previous echocardiographic studies, CMR demonstrated transient RV systolic dysfunction immediately after a marathon that recovered within weeks. The absence of delayed enhancement of the myocardium using CMR also revealed no evidence of permanent injury due to the strenuous exercise of full marathon running. Whether transient RV systolic dysfunction occurs in the setting of a shorter distance such as a half marathon, however, remains ill defined.


The objectives of the current study were twofold: (1) to assess the extent and severity of changes in RV function following the completion of a half marathon, using serial cardiac biomarkers, RT3DE, and CMR, and (2) to determine the accuracy of RT3DE for determining RV dysfunction after a half marathon compared with CMR.


Methods


Study Population


A prospective study involving 15 healthy, nonelite volunteers participating in the 2009 Manitoba Half Marathon was performed. Subjects aged 18 to 40 years who completed the race were included. Patients with histories of coronary artery disease, hypertension, smoking, elevated lipids, diabetes, and/or contraindication to undergo CMR were excluded.


Cardiac Biomarkers


Myoglobin, CK, and cTnT were evaluated at three separate time points: (1) 1 week before the race, (2) immediately after the race, (3) and 1 week after the race. Myoglobin and CK levels were determined using a Roche Elecsys and a Roche 917 analyzer, respectively (Roche Diagnostics GmbH, Mannheim, Germany). Quantitative determination of cTnT levels was performed using a third-generation Roche Elecsys assay.


Echocardiography


All subjects underwent baseline transthoracic echocardiographic (TTE) imaging 1 week before the race, immediately following the race, and 1 week after race completion. Following completion of the half marathon, each patient was immediately transferred to the study hospital for performance of the TTE exam. The transfer time from the half marathon site to the study hospital was 10 min. All TTE studies were performed immediately upon arrival at the study hospital. All patients underwent TTE imaging using a GE Vivid 7 (GE Healthcare, Milwaukee, WI) at each time point. Left ventricular (LV) and left atrial cavity dimensions indexed to body surface area were determined from two-dimensional images in accordance with the guidelines of the American Society of Echocardiography. RV cavity dimensions, RV fractional area change (FAC), and tricuspid annular plane systolic excursion (TAPSE) were also determined. Continuous-wave Doppler was used to measure the peak velocity across the tricuspid valve, and the maximal pulmonary arterial systolic pressure was estimated using the simplified Bernoulli equation.


Real-time three-dimensional TTE imaging was performed using a dedicated broadband, wide-angle, matrix-array transducer to acquire the entire RV cavity within the pyramidal scan volume. Acquisition of full-volume data sets was triggered to the R wave of every cardiac cycle to allow for an acquisition time of four heartbeats during an adequate breath hold. The subvolumes were automatically stitched to a sequence of full three-dimensional volumes covering the entire right ventricle and stored digitally for offline analysis using TomTec software (TomTec Imaging Systems, Unterschleissheim, Germany), as previously described.


CMR


CMR was performed on all study participants at baseline and within 24 hours of completion of the half marathon using a 1.5-T scanner (Avanto; Siemens Medical Solutions, Erlangen, Germany). Specifically, following acquisition of the TTE images after the half marathon, each participant underwent CMR on an hourly basis, until all 15 studies were completed. Cine balanced steady-state free-precession short-axis images then encompassed the entire left ventricle from the base to the apex (stack of 10 sequential short-axis slices; repetition time, 64 ms; echo time, 1 ms; flip angle, 80°; slice thickness, 8 mm; interslice gap, 1.6 mm; matrix size, 192 × 132) to obtain the LV ejection fraction. To evaluate for myocardial edema, dark-blood T2-weighted turbo spin-echo short-axis images were obtained (repetition time, 1800–2100 ms; echo time, 74 ms; slice thickness, 8 mm; interslice gap, 4 mm; matrix size, 256 × 175). Late gadolinium enhancement images were obtained after 10 min of 0.2 mmol/kg injection of gadolinium diethylenetriamine pentaacetic acid (Magnevist; Schering AG, Berlin, Germany) using a T1-weighted inversion recovery–prepared multislice true fast imaging with steady-state precession sequence with magnitude and phase-sensitive reconstruction. Images were acquired sequentially in the short axis, followed by horizontal and vertical long-axis images (repetition time, 700 ms; echo time, 1.0 ms; flip angle, 40°; slice thickness, 8 mm; interslice gap, 1.6 mm; matrix size, 192 × 144). Quantitative analysis was performed using dedicated computer software (CMR 42 release 3.1.2; Circle Cardiovascular Imaging, Calgary, AB, Canada).


Statistical Analysis


Data are summarized as mean ± SD, number (percentage), or median (interquartile range). Paired Student’s t tests were used to compare continuous variables. Chi-square and Fisher’s exact tests were applied to compare categorical variables. One-way analysis of variance (nonparametric with Dunn testing) was used to compare baseline, immediate, and 1-week postrace cardiac biomarker and echocardiographic values. Linear regression analysis and Bland-Altman plots were used to compare RV volumes and RVEF between the various imaging modalities. The Bland-Altman method is a plot of the differences of the data on a chart with mean difference ± 1.96 × standard deviation of the differences. The 95% agreement limits are ±1.96 × standard deviation of the differences. Agreement between intraobserver and interobserver variability of the LV volumes and LV ejection fraction between the imaging modalities was computed from the absolute differences between repeated measurements using the Mann-Whitney U test. P values < .05 were considered statistically significant. SAS version 8.01 (SAS Institute Inc., Cary, NC) was used to perform the analysis.




Results


Of the 3,953 amateur athletes (1,971 men; mean age, 35 ± 13 years) who completed the 2009 Manitoba Half Marathon, the mean finishing time was 137 ± 26 min. Our study population of 15 participants (seven men; mean age, 32 ± 6 years) completed the half marathon with an average finishing time of 130 ± 24 min. The start time of the Manitoba Half Marathon was 7 am , and each study participant underwent TTE imaging 10 min after crossing the finish line. The first CMR was scheduled at 9 am , and subsequent exams were performed on an hourly basis until all 15 participants had completed the study. The mean heart rates at the time of the TTE and CMR exams after the race were 97 ± 11 and 71 ± 12 beats/min, respectively. The patients were mildly trained, with a mean training distance of 19 ± 11 mi/week and a mean training time of 5 ± 3 hours/week for the 14 ± 6 weeks before the half marathon. Of the 15 subjects, only three had previously participated in a marathon. All 15 participants drank fluids freely during the race. The weights of the subjects did not change significantly after the half marathon ( Table 1 ).



Table 1

Patient clinical characteristics ( n = 15)








































Characteristic Baseline After the race
Age (y) 22–39
Gender
Male 7 (47%)
Female 8 (53%)
Weight (kg) 70 ± 11 70 ± 11
Heart rate (beats/min) 66 ± 13 97 ± 11
SBP (mm Hg) 132 ± 13 118 ± 13
DBP (mm Hg) 74 ± 6 68 ± 4

Data are expressed as range, as number (percentage), or as mean ± SD.

DBP , Diastolic blood pressure; SBP , systolic blood pressure.


Myoglobin, CK, and cTnT levels were all normal at baseline ( Table 2 ). After completion of the half marathon, myoglobin and CK levels increased significantly compared with baseline ( Table 2 ). Although myoglobin and CK are not cardiac specific, they do indicate the strenuous nature of a half marathon. Immediately after completing the half marathon, all patients demonstrated elevated cTnT levels, with a median value of 0.37 ng/mL (interquartile range, 0.22–0.68 ng/mL). Myoglobin, CK, and cTnT levels had normalized at 1-week follow-up in all patients.



Table 2

Summary of serial cardiac biomarkers for total population ( n = 15)
























Characteristic Baseline After the race 1 week after the race
Myoglobin (mg/L) 25 (18–82) 698 (552–2,100) 65 (44–88)
CK (U/L) 120 (117–190) 625 (441–1,922) 210 (156–462)
cTnT (ug/L) <0.01 0.37 (0.26–0.74) <0.01

Data are expressed as median (interquartile range).

P < .05, after the race vs baseline.



LV dimensions, volumes, and ejection fractions remained unchanged from baseline to after the half marathon ( Table 3 ). However, right atrial volume increased from 41 ± 12 mL at baseline to 57 ± 14 mL after the race ( P < .05; Table 3 ). Compared with baseline values, RV FAC by two-dimensional TTE imaging decreased significantly (41 ± 2% vs 33 ± 4%, P < .05). TAPSE was significantly decreased compared with baseline values (2.7 ± 0.4 vs 1.7 ± 0.4 cm, P < .05). Both RV FAC and TAPSE values returned to normal 1 week after the half marathon. There was an increase in pulmonary arterial systolic pressure, from 14 ± 4 mm Hg at baseline to 44 ± 3 mm Hg immediately after the half marathon ( P < .05).



Table 3

Echocardiographic data in the patient population ( n = 15)




















































































































































Echocardiographic parameter Baseline After the race Follow-up P
LV parameters (2D TTE)
LVEDD (mm) 51 ± 5 50 ± 4 51 ± 3 .94
LVESD (mm) 32 ± 6 32 ± 5 33 ± 4 .76
LVEDV (mL) 115 ± 17 112 ± 15 108 ± 28 .65
LVESV (mL) 39 ± 12 41 ± 23 40 ± 14 .54
IVS (mm) 9 ± 1 8 ± 1 9 ± 2 .65
PWT (mm) 9 ± 1 8 ± 1 9 ± 2 .49
LVEF (%) 64 ± 3 62 ± 6 63 ± 4 .63
LV mass/BSA (g/m 2 ) 101 ± 12 102 ± 22 98 ± 18 .52
LA parameters (2D TTE)
LA diameter (mm) 37 ± 3 37 ± 2 36 ± 5 .64
LA volume (mL) 43 ± 12 45 ± 15 41 ± 11 .42
RA and RV parameters (2D TTE)
RA volume (mL) 41 ± 12 57 ± 14 38 ± 12 <.05
RVEDD (mm) 31 ± 2 41 ± 2 30 ± 3 <.05
RV diastolic area (mm 2 ) 13 ± 4 17 ± 2 12 ± 3 <.05
RV systolic area (mm 2 ) 7 ± 2 11 ± 4 6 ± 2 <.05
RV FAC (%) 41 ± 2 33 ± 4 41 ± 5 <.05
TAPSE (mm) 2.7 ± 0.4 1.7 ± 0.3 2.6 ± 0.4 <.05
RV parameters (RT3DE)
RVEDV (mL) 125 ± 26 186 ± 24 125 ± 23 <.05
RVESV (mL) 50 ± 18 100 ± 21 52 ± 19 <.05
RVEF (%) 59 ± 4 45 ± 5 58 ± 4 <.05

Data are expressed as mean ± SD.

BSA , Body surface area; IVS , interventricular septum; LA , left atrial; LVEDD , LV end-diastolic diameter; LVEDV , LV end-diastolic volume; LVEF , LV ejection fraction; LVESD , LV end-systolic diameter; LVESV , LV end-systolic volume; PWT , posterior wall thickness; RA , right atrial; RVEDD , RV end-diastolic diameter in parasternal long-axis view; RVEDV , RV end-diastolic volume; RVESV , RV end-systolic volume; TTE , transthoracic echocardiography; 2D , two-dimensional.

P < .05, after the race vs baseline.



Similarly, RV volumes increased and systolic function decreased following the half-marathon using RT3DE ( Table 3 ). RV end-diastolic volume increased from 125 ± 26 mL at baseline to 186 ± 24 mL after the half marathon. RV end-systolic volume increased from 50 ± 18 mL at baseline to 100 ± 21 mL after the half marathon. Finally, the RVEF by RT3DE decreased from 59 ± 4% at baseline to 45 ± 5% immediately following the race ( P < .05; Table 3 ). At 1 week follow-up, RV volumes and RVEF by RT3DE had returned to baseline values.


RV volumes and function were abnormal on CMR after the marathon, which paralleled our echocardiographic findings. RV end-diastolic volume increased after the marathon (135 ± 24 vs 195 ± 21 mL, P < .05), and the RVEF was reduced, at 47 ± 5% compared with 60 ± 2% at baseline ( P < .05) ( Table 4 ). As shown in Figure 1 , there were strong linear correlations between RVEF as assessed by RT3DE and CMR at baseline and after the half marathon ( r = 0.69 and r = 0.87, P < .01, respectively). There was no evidence of myocardial edema on T2 imaging or delayed enhancement of the LV myocardium, even though all patients demonstrated elevated cTnT levels at the time of CMR.



Table 4

CMR data in the patient population after the marathon ( n = 15)




































































































CMR parameter Before the marathon After the marathon
LV parameters
LVEDD (mm) 51 ± 4 50 ± 5
LVESD (mm) 30 ± 9 30 ± 4
LVEDV (mL) 157 ± 22 161 ± 18
LVESV (mL) 51 ± 11 55 ± 13
LVEDV/BSA (mL/m 2 ) 83 ± 10 87 ± 8
LVESV/BSA (mL/m 2 ) 26 ± 12 27 ± 15
IVS (mm) 9 ± 1 9 ± 1
PWT (mm) 9 ± 1 9 ± 2
LVEF (%) 66 ± 5 68 ± 3
LV mass (g) 218 ± 25 212 ± 16
LV mass/BSA (g/m 2 ) 123 ± 14 117 ± 11
LA parameters
LA diameter (mm) 36 ± 3 37 ± 5
LA volume (mL) 42 ± 13 41 ± 16
LA volume/BSA (mL/m 2 ) 27 ± 6 25 ± 4
RA and RV parameters
RA volume (mL) 40 ± 9 56 ± 12
RVEDD (cm) 32 ± 6 43 ± 6
RVEDV (mL) 135 ± 24 195 ± 21
RVEF (%) 60 ± 2 47 ± 5
RV mass (g) 66 ± 3 65 ± 4
RV mass/BSA (g/m 2 ) 33 ± 3 34 ± 3

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Jun 15, 2018 | Posted by in CARDIOLOGY | Comments Off on The Role of Three-Dimensional Echocardiography in the Assessment of Right Ventricular Dysfunction after a Half Marathon: Comparison with Cardiac Magnetic Resonance Imaging

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