Regular moderate physical activity confers multiple health benefits (5,9,36). More extreme forms of exercise (e.g., marathon running), on the other hand, represent a major challenge to cardiovascular physiology and momentarily increases the risk to adverse cardiovascular events including sudden cardiac death (36). This “paradox of exercise” (22) has stimulated research into the immediate effects of prolonged physical exertion on various aspects of cardiac function.
Exercise alters the autonomic tone. This has been demonstrated by studying changes in HR, HR recovery, and HR variability (HRV) as noninvasive measures of cardiac autonomic regulation: individuals who perform regular endurance training generally have a lower resting HR, a faster HR recovery, and increased HRV compared with sedentary individuals (11,35). However, the acute autonomic response to prolonged exercise is not well studied, particularly the time course of change in association with physical exertion and postexertional rest.
Previous research has also demonstrated a range of transient biochemical, echocardiographic, and electrophysiological alterations after endurance exercise (25,31). For example, the myocardial damage marker troponin rises in a large proportion of participants (34). Yet, whether such troponin elevation reflects a physiologic response to prolonged stress or potentially detrimental cardiac effects is subject to debate (12,24).
We hypothesized that the degree of troponin increase after strenuous exercise may reflect the magnitude of exercise-induced cardiovascular stress. Therefore, we investigated the effect of completing a 30-km long-distance running race on autonomic tone and associations with postexertional increases in high-sensitivity cardiac troponin (hsTnT) and other parameters of cardiac function. To compare postrace findings with stable baseline values and because we hypothesized that prolonged exercise would cause long-lasting changes in autonomic tone, HR, HRV, and arrhythmias were recorded continuously from 2 d before until 4 d after the race using a dedicated monitor. Because the response to exercise may vary with age, gender, and previous race experience (30), we focused on middle-age male first-time participants. This group is rapidly growing (2) and is considered to be at highest risk for exercise-induced adverse cardiovascular events (36).
The study was performed in association with the world’s largest cross-country running race, Lidingöloppet, held annually in the hilly terrain on the island of Lidingö outside Stockholm. All males age ≥45 yr, who registered in 2010 for first-time participation in a 30-km event, and who, for logistical reasons, lived in the greater Stockholm area were invited. Individuals who had participated two times or more in any other endurance race ≥10 km during the last 2 yr were excluded. Because of a limited number (n = 43) of available HR monitors (HRM), they were randomly assigned among eligible subjects. The study protocol adhered to the declaration of Helsinki and was approved by the regional ethical review board. All participants provided written informed consent before study participation.
Pre- and postrace cardiac examination.
A detailed evaluation was performed within 3 wk before the race and included standardized questionnaires to quantify previous and current exercise training, cigarette smoking, and medication and nutritional supplement use; a structured medical history and physical examination (23); a 12-lead ECG; blood tests; and echocardiography. This was done for study purposes (1); preparticipation evaluation is neither mandatory nor routine in Sweden. Subjects were instructed not to train on or on the day before the prerace examination day.
On the race day, weight was measured before and after the race and the body mass index (BMI) (body weight in kilogram per height in meter squared) was calculated accordingly. A 12-lead ECG was recorded within 1.0 ± 0.9 h after the race.
Blood was collected from the antecubital vein pre- and postrace, and all blood samples were analyzed within 3 h without prior freezing. Samples were analyzed for hsTnT, hemoglobin, hematocrit, creatinine, sodium, and potassium. The Van Beaumont formula (percentage change in plasma volume = 100 (prerace hematocrit − postrace hematocrit)/postrace hematocrit × 1/(1 − prerace hematocrit)) was used to correct for race-induced changes in plasma volume. Normal ranges of laboratory values were determined according to local laboratory standards.
All subjects underwent pre- and postrace transthoracic echocardiography (VIVID E9 or VIVID 7; GE-Vingmed Ultrasound AS, Horten, Norway) using views and measurements recommended by the American Society of Echocardiography (ASE) (20). A dedicated EchoPAC (version 7.0, GE-Vingmed Ultrasound AS) workstation was used for postacquisition analyses. Cardiac dimensions including left ventricular mass (LVM) were obtained in a two-dimensional parasternal long axis view and indexed for body surface area as indicated by the letter I (e.g., LVMI). LV hypertrophy was defined as LVMI >115 g·m−2. Eccentric morphology was defined as a relative wall thickness = (left ventricular posterior wall thickness + left ventricular septal wall thickness)/left ventricular end-diastolic diameter ≤0.42 as per ASE guidelines (20). The E/A ratio was calculated from the mitral inflow E and A wave velocities. Tissue velocities, including peak systolic (Sm), early diastolic (Em), and late diastolic lengthening velocity (Am), were recorded from the median of three cardiac cycles using color-coded tissue Doppler in the basal septum.
Interobserver (PA, AS) and intraobserver (PA) reproducibility was tested in a random sample (n = 26). Interobserver coefficient of variation was 9.4% (95% confidence interval (CI), 7.7–11.1) and 10.4% (95% CI, 6.5–14.3) for cardiac dimensions and tissue velocity imaging, respectively. Intraobserver coefficient of variation was 7.2% (95% CI, 4.7–11.1) and 8.1% (95% CI, 5.1–11.1) for cardiac dimensions and tissue velocities, respectively.
All subjects were equipped with a wireless HRM (AVIVO™ Mobile Patient Management System, Corventis Inc.) 2 d before the race. The device has been described in detail elsewhere (4). In summary, the monitor is lightweight (20 g), leadless, and water resistant and thus suitable for use in conjunction with physical activity. HR was continuously monitored and reported by the monitor as the median for each 5-min interval during the monitoring period. Any missing data were replaced by the mean of the preceding and after 5-min median HR values. To control for the effects of daily living activity and sports (27), we compared HR values during nighttime (2:00–4:00 a.m.) when participants were assumed to be in a similar state of rest.
HRV was calculated as the SD of the mean of normal sinus intervals in all 5-min segments during a 24-h period (SDANN) and is presented either as the daily mean value or as the moving average over the 12 h before and after each time point.
The HR and HRV recordings from 48 to 24 h before the race are called baseline. The time to return of HRV to baseline levels was determined in each individual as the time from the end of the race until the 95% CI of the postrace HRV moving average overlapped with the 95% CI of the baseline HRV, or as the end of the recording period if HRV did not return to baseline.
Individual HR reserve (HRR) (HRR = maximum HR − resting HR) (17) was calculated in all subjects. Maximum HR was determined according to the following formula: maximum HR = 220 − age (10), or as the highest achieved HR during the study period (whichever was highest). Resting HR was taken at the prerace examination after 5 min of supine rest. Postrace HR was measured 30 min after race completion. Running intensity was measured as the mean percentage of HRR used during the race. Postrace HR recovery was measured as the percentage of HRR used 30 min after the race.
The monitor also recorded atrial and ventricular arrhythmias. Episodes of atrial fibrillation were manually excluded from HR and HRV analyses.
Descriptive data were assessed for normal distribution and homogeneity of variance by the Kolmogorov–Smirnov and Levine test, and are presented as mean ± SD or median (interquartile range), where appropriate. Correlations were assessed by Pearson r or Spearman rho. The independent t-test or the Mann–Whitney U tests were used to compare groups. When comparing multiple means, one-way ANOVA or the Kruskal–Wallis test was applied. Within-group differences between pre- and postrace values were assessed with a paired samples t-test or the Wilcoxon test.
A multivariate regression model (enter method), including factors that correlated significantly with postrace change in HRV, was used to test independent associations.
All statistical analyses were performed using PASW Statistics version 20 (IBM Corporation, Armonk, NY). A P value of <0.05 was considered statistically significant.
Of 93 eligible subjects, 43 were randomly assigned to receive a wireless cardiovascular monitor. One monitor was lost during the race. Thus, data from 42 subjects form the basis for the present study. On the race day, temperature ranged from 14°C to 20°C with overcast skies.
Pre- and postrace examination.
Results from the prerace (9 ± 5 d) and postrace evaluation (1.05 ± 0.80 h) are given in Table 1. One runner did not attend the postrace examination. No subjects reported current smoking, and there was no history of diabetes mellitus or previous cardiovascular events in any participant. Four runners (10%) reported sedentary behavior (<30 min of physical activity ≤3 times per week) and another four reported taking medications (angiotensin-converting enzyme inhibitors (n = 2), angiotensin receptor blocker and statin (n = 1), and statin only (n = 1)). The mean weight loss during the race was 1.1 ± 0.9 kg. Notably, although all subjects had normal hsTnT levels prerace, postrace levels were above the value clinically used as diagnostic threshold for myocardial damage (>14 ng·L−1) in all but one (97%). There was no significant correlation between changes in hsTnT levels and changes in plasma volume as estimated from change in hematocrit. No subject had signs of acute ischemia on postrace 12-lead ECG recordings.
All participants were in sinus rhythm at the prerace examination and during the prerace study period. No sustained ventricular arrhythmias occurred, but atrial fibrillation was recorded in two runners during postrace monitoring (one episode of 272 min and three episodes lasting 33–105 min, respectively). Missing HR data during the prerace, in-race, and postrace periods were 1.3%, 17.8%, and 1.5%, respectively. No subject had >2% missing HR data during the pre- and postrace periods.
The mean HR during the entire study period (48 h before until 102 h after the race) was 64 ± 7 bpm. Mean daily HR did not vary between study days, except for a significantly higher HR on the day of the race (Fig. 1).
During the race, runners reached a mean HR of 127 ± 14 bpm, corresponding to a mean relative running intensity of 55% ± 6% of HRR. Runners reached an average maximum HR of 166 ± 15 bpm. Thirty minutes after the race HR had recovered to 104 ± 18 bpm corresponding to an HRR use of 37% ± 9%.
The night-time HR (recorded 2:00–4:00 a.m.) was 54 ± 8 bpm during the two nights before the race, significantly increased to 64 ± 9 bpm (P = 0.002) during the first night postrace, and then returned to prerace levels during the second night postrace (55 ± 9 bpm, P = 0.67).
The time course of the moving HRV average is shown in Figure 2. Compared with the duration of HR increase postrace, HRV showed a more protracted reduction before returning to prerace levels. Mean HRV was 149 ± 7 ms at baseline, markedly increased during the race day with a peak of 248 ± 72 ms. After race completion, HRV fell below baseline values with a trough (104 ± 22 ms) at 16 h postrace. This was followed by a rebound, peaking approximately 26 h postrace, and then a gradual return toward baseline values. This general pattern was observed in all subjects. The median time to return to baseline HRV was 64 h (51–102 h). In seven (17%) subjects, lower than baseline HRV persisted throughout the postrace follow-up.
Compared with baseline, mean HRV was significantly lower on day 1 (−18 ± 16 ms, P < 0.001) and day 2 (−21 ± 20 ms, P = 0.018) after the race. There was a trend toward lower than baseline HRV also on day 3 (−15 ± 28 ms) and 4 (−10 ± 25 ms) postrace that did not reach statistical significance.
A higher resting HR correlated with a larger HRV reduction on day 1 after the race (r = −0.66, P < 0.001), a greater increase in nighttime HR on day 1 postrace (r = 0.41, P = 0.03), and use of a higher proportion of HRR (higher running intensity) during the race (r = 0.42, P = 0.008). Higher running intensity also correlated with a higher night-time HR on the night after the race (r = 0.37, P = 0.04).
A larger HRV reduction on day 1 after the race was observed in runners with higher resting HR (see above) and higher postrace hsTnT (r = −0.49, P = 0.003). A larger HRV reduction was also weakly associated with a lower amount of training hours per week (r = 0.35, P = 0.02) and a higher relative mean running intensity (r = −0.33, P = 0.04). Importantly, in a multivariate model (Table 2) including these parameters, higher postrace hsTnT remained significantly associated with reduced postrace HRV (β = −0.48, P = 0.01). The relation between quartiles of absolute change in HRV on day 1 and postexertional hsTnT levels is shown in Figure 3.
In addition to the association between elevated hsTnT and decreased HRV after the race, higher postrace hsTnT also correlated with a higher mean running intensity (r = 0.44, P = 0.006) and less HR recovery at 30 min postrace (r = 0.48, P = 0.005). The quartile of runners with the least HR recovery at 30 min postrace had twice as high postrace hsTnT levels compared with the quartile with fastest HR recovery (64 (32–79) vs 31 (20–51), P = 0.04).
Echocardiographic measures of ejection fraction, longitudinal velocities, and diastolic parameters did not correlate with changes in HR, HRV, or troponin, nor did age, BMI, runtime, changes in body weight, hemoglobin, creatinine, or electrocardiographic waveform measures (QRS, QT, and QTcB). Repeated analyses after excluding the four subjects on cardiovascular medication did not significantly alter our findings.
This study aimed to characterize the time course and pattern of change in autonomic control, reflected by HR and HRV (SDANN), in middle-age male first-time long-distance running race participants. Furthermore, possible associations with hs-TNT and other cardiovascular parameters including echo- and electrocardiography were assessed. Compared with baseline values obtained from monitoring during normal conditions before the race, HR was increased during the night after the race, whereas HRV remained decreased for several days, indicating an extended period of attenuated HRV.
A novel observation was the strong association between reduced postexertional HRV and elevated levels of cardiac troponin, which remained significant also after multivariable adjustment. Although postexertional troponin elevation per se was a uniform phenomenon—in fact, hsTnT reached levels indicative of myocardial damage in all but one subjects—our data demonstrate that the magnitude of response differs between individuals: participants with a larger increase in hsTnT also had a greater degree of postexertional autonomic alteration.
HR was only increased during the night after the race, whereas HRV remained below baseline values for several days. This period of altered autonomic activity was longer compared with a report by Hautala et al. (13) who studied nine athletes after 75 km of cross-country skiing and found that cardiac vagal outflow was restored only a few hours after race completion and followed by enhanced vagal regulation the day after the race. However, the latter study included younger athletes (mean age, 36 yr) who may have been better accustomed to the challenge of endurance exercise than the older and inexperienced runners in our study. In fact, although our inclusion criteria (novice middle-age runners) attempted to limit the effect of age (6) and previous endurance experience (11) on autonomic regulation, some heterogeneity with regard to fitness level remained. As expected (11), better fitness (e.g., lower resting HR, less use of HRR during the race), predicted runners with a less pronounced HR elevation during the night after the race as well as runners with a less pronounced postrace decrease in HRV.
It is conceivable that an increase in HR is a response to increased sympathetic activation in the setting of impaired cardiac mechanical functioning and/or exercise-induced dehydration. However, weight loss during the race (as a proxy for intravascular volume loss) did not correlate with changes in HR (nor with HRV changes), although individual differences in fluid redistribution from the intra- to the extravascular compartment cannot be excluded (26). Thus, the changes in HR and HRV after the race may represent true alteration of autonomic balance, with increased sympathetic tone and or parasympathetic withdrawal.
Endurance exercise may cause decreased cardiac systolic and diastolic function (“cardiac fatigue”) postrace (25,31). In the present study, although echocardiographic measurements obtained by conventional Doppler (E/A) as well as tissue Doppler (Em) did indeed change postrace, the true nature of the values obtained is difficult to interpret. The difference detected in body weight suggests altered cardiac loading was present postrace, and the associated relatively large increase in HR (mean +17 bpm) is likely to have considerable effect on cardiac longitudinal function. Future studies should therefore carefully control for altered loading conditions and HR when investigating “cardiac fatigue” in athletes.
During the hours before the race, there was a gradual decrease in HRV. As our subjects all lived in the Stockholm area without a need for long-distance travelling or changing accommodation, this pattern may reflect psychoemotional components (i.e., precompetitive anticipatory excitement) affecting cardiac autonomic regulation.
The episodes of atrial fibrillation registered after the race are compatible with the increased incidence of atrial fibrillation in endurance athletes (3) and is also in line with the influence of autonomic modulation in atrial fibrillation onset (8).
All but one subject in this study had elevated levels of troponin after the race. This is in keeping with findings from a meta-analysis describing a high prevalence of elevated cardiac troponin after exercise (interstudy variation may largely depend on the timing of postrace blood sampling) (34). The mechanism underlying postexertional troponin elevation remains unknown. Several theories, including transmembrane leakage of cytosolic troponin (15), stretch-related integrin-mediated release (14,32), and decreased renal troponin clearance (37), have been proposed. Cross-reactivity with skeletal troponin is unlikely as the newer troponin assays are specific for cardiac troponin even in the presence of severe skeletal muscle damage (28,33). The clinical significance of postexertional troponin elevation is contested. One report suggests that this phenomenon is physiologic (24), whereas others have shown that postexertional troponin levels correlate with the degree of exercise-induced right ventricular dysfunction (18) and that troponin levels after stress test-induced myocardial ischemia predict the presence of CAD (29).
Importantly, we found a significant relation between changes in HRV and concentrations of hsTnT: troponin levels were higher in subjects with larger postrace HRV reduction, in those with higher relative running intensity, and in those with reduced HR recovery after the race. The latter association may raise concern because poor HR recovery after exercise testing is prognostically unfavorable (7) also in middle-aged men without known cardiac disorders (16).
The significant association between postexertional HRV changes and troponin levels remained significant after multivariable analysis. Our data do not necessarily indicate that exercise-related autonomic changes per se leads to TnT release given that similar biophysical factors predispose both to cardiac autonomic alterations and elevated biomarker release. Nonetheless, our findings do provoke important questions whether these phenomena are entirely physiological and benign in the setting of endurance exercise. At present, it cannot be excluded that the magnitude of change in these parameters may carry clinically important information for the purpose of identifying individuals less suited for this type of strenuous physical activity. As elevated troponin, reduced HRV and reduced HR recovery are all well-established cardiovascular risk markers under many other types of circumstances (19,21,29,38). This is a line of study that will need to be investigated further. However, although the present report is relevant for the conception and execution of such studies, it should be noted that both troponin elevation and autonomic alterations appear only after exertion. Accordingly, these tests will not allow athletes to be stratified before commencing exercise.
For methodological reasons, HRV could only be analyzed in the time domain (SDANN), thus precluding separation of sympathetic and parasympathetic contributions to HRV. Furthermore, it is possible that the effect of prerace mental excitement may have influenced autonomic regulation, although we tried to control for this by monitoring for 48 h prerace.
We only measured troponin at a single time point after the race. Because exercise-induced troponin elevation is transient (31), it is possible that our measurements do not reflect true peak values. However, this methodological limitation would most likely lead to a type II error, i.e., missing an association between postexertional troponin levels and other parameters of cardiac function.
Furthermore, although this is the largest study to date assessing the time course of HRV adaptation after endurance exercise, there was limited statistical power in the multivariate analyses. Finally, we included only males ≥45 yr, and results may not be extrapolated to other populations.
Participation in a 30-km cross-country running race caused marked and prolonged alterations in autonomic control reflected by an increase in night-time HR and reduced HRV after the race. Notably, more pronounced autonomic alterations were associated with higher levels of postexertional hsTnT, the magnitude of which may thus reflect the level of exercise-induced cardiovascular stress. In light of these findings, an appropriate rest period after prolonged strenuous exercise appears prudent to allow for complete recovery. This may be particularly important in older and less fit individuals, as autonomic changes appear to be larger in this group.
This work was supported by grants from the Swedish Heart and Lung Foundation and the Swedish Centre for Sports Research. HRM was provided by courtesy of Corventis Inc.
There are no conflicts of interest in this study.
The results of the present study do not constitute endorsement by the American College of Sports Medicine.
We are indebted to Eva Wallgren and the staff of the Cardiovascular Research Unit and to Peter Matha and his group at the Clinical Trial Centre, both from the Karolinska University Hospital, who provided invaluable technical and logistic support.
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Keywords:© 2014 American College of Sports Medicine
HEART RATE; HEART RATE VARIABILITY; HEART RATE RECOVERY; EXERCISE; MASTER ATHLETES; TROPONIN