ORIGINAL RESEARCH
Sex Differences in Cardiac Function After Prolonged Strenuous Exercise Anita T. Cote, PhD,* Aaron A. Phillips, PhD,*† Heather J. Foulds, MSc,*† Sarah A. Charlesworth, PhD,* Shannon S.D. Bredin, PhD,* Jamie F. Burr, PhD,‡ Michael S. Koehle, MD, PhD,§¶ and Darren E.R. Warburton, PhD*†
Objective: To evaluate sex differences in left ventricular (LV) function after an ultramarathon, and the association of vascular and training indices with the magnitude of exercise-induced cardiac fatigue.
Design: Descriptive field study. Setting: Fat Dog 100 Ultramarathon Trail Race, Canada. Participants: Thirty-four (13 women) recreational runners (aged
Regression analysis found that higher baseline arterial compliance was associated with lower reductions in cardiac function postexercise, to which sex was a significant factor for E0 of the lateral wall. Faster race pace and greater lifetime ultramarathons were associated with lower reductions in LV longitudinal strain (P , 0.05).
Conclusions: Cardiac responses after an ultramarathon were similar between men and women. Greater evidence of exerciseinduced cardiac fatigue was found to be associated with lower baseline arterial compliance and training status/experience.
28-56 years).
Clinical Relevance: These findings suggest that vascular health is
Interventions: A 100-km or 160-km mountain marathon.
an important contributor to the degree of cardiovascular strain incurred as the result of an acute bout of prolonged strenuous exercise.
Main Outcome Measures: Baseline baroreceptor sensitivity, heart rate variability, and arterial compliance; Pre-exercise and postexercise echocardiographic evaluations of LV dimensions, volumes, Doppler flow velocities, tissue velocities, strain, and strain rate.
Key Words: cardiac fatigue, ultraendurance exercise, echocardiography (Clin J Sport Med 2015;25:276–283)
Results: Finishers represented 17 men (44.8 6 6.6 years) and 8
women (45.9 6 10.2 years; P = 0.758). After ultraendurance exercise, significant reductions (P , 0.05) in fractional shortening (men: 40.9 6 6.9 to 34.1 6 7.6%; women: 42.5 6 6.5 to 34.6 6 7.9%) diastolic filling (E/A, men: 1.28 6 0.68 to 1.26 6 0.33; women: 1.55 6 0.51 to 1.30 6 0.27), septal and lateral tissue velocities (E0 ), and longitudinal strain (men: 221.02 6 1.98 to 218.44 6 0.34; women: 220.28 6 1.90 to 218.44 6 2.34) were observed. Sex differences were found for baseline cardiac structure and global function, peak late transmitral flow velocity, and estimates of LV filling pressures (P , 0.05). Submitted for publication September 11, 2013; accepted March 18, 2014. From the *Cardiovascular Physiology and Rehabilitation Laboratory, University of British Columbia, Vancouver, Canada; †Experimental Medicine Program, Faculty of Medicine, University of British Columbia, Vancouver, Canada; ‡Applied Human Sciences, University of Prince Edward Island, Charlottetown, Canada; §Environmental Physiology Laboratory, School of Kinesiology, University of British Columbia, Vancouver, Canada; and ¶Division of Sports Medicine, University of British Columbia, Vancouver, Canada. Supported by the Canadian Institutes of Health Research, Michael Smith Foundation for Health Research, Canada Foundation for Innovation, National Science and Engineering Research Council, and the British Columbia Knowledge & Development Fund. D. E. R. Warburton was supported by salary awards from the Canadian Institutes of Health Research and the Michael Smith Foundation for Health Research. All authors report no conflicts of interest. Corresponding Author: Darren E.R. Warburton, PhD, Unit II Osborne Centre, 6108 Thunderbird Blvd, University of British Columbia, Vancouver, BC V6T 1Z3, Canada ([email protected]). Copyright © 2014 Wolters Kluwer Health, Inc. All rights reserved.
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INTRODUCTION Exercise-induced cardiac fatigue is characterized by a reduction in left ventricular (LV) systolic and diastolic function subsequent to exercise in healthy humans,1 particularly prolonged strenuous exercise (PSE).2 These reductions in LV performance have been found to occur despite the absence of underlying cardiovascular pathologies3–6 and seem to be transient in nature with normal function restored typically within 48 hours7 However, the clinical relevance of exercise-induced cardiac fatigue warrants further study,8–10 particularly considering the appreciable increase in ultraendurance participation over recent years.11 The average age of winning ultramarathoners is older than the typical age of winning marathoners.12 This may be interpreted that to perform well in ultraendurance events, accumulating greater years of training may be beneficial, although the cumulative effects of chronic PSE on the cardiovascular system is unclear.13 The juxtaposition of low mortality rates and excellent functional capacity in lifelong exercisers, alongside reports of adverse structural and electrical cardiac remodeling,14,15 brings into question the risks involved with lifelong, high-volume endurance training. Another emerging trend is the increase in female participants in ultraendurance events where female finishers increased 20% in a 4-year span.16 Despite this increase in female competitors, the literature to date has yielded limited Clin J Sport Med Volume 25, Number 3, May 2015
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information regarding the cardiovascular consequences of PSE in women. Previous work from our research group found males experienced greater reductions in LV systolic function as a consequence of a half-ironman triathlon compared with female competitors,17 the mechanisms of which are not known. Prolonged strenuous exercise has been shown to significantly increase plasma catecholamines,18 a marker of sympathetic activity. Phenotypical evidence of sex differences in cardiac norepinephrine transporter function19 suggests that males exhibit differences in cardiac-specific sympathetic activity. Although, women typically display greater parasympathetic control of heart rate (HR) than men at rest, considered to be a reflection of the enhanced cardioprotection characteristic of healthy pre-menopausal females,20 sympathovagal balance of women may be more vulnerable to the effects of strenuous exercise than men.21,22 Thus, how sex may influence the cardiac responses to significant physiological stress, such as PSE, is not clear. As a means to address this question, assessment of regional myocardial function, such as strain and strain rate (SR) imaging, will provide a thorough analysis of LV function.23 In addition, spontaneous measures of cardiovagal baroreflex sensitivity (BRS) can provide a noninvasive indication of autonomic modulation with exercise.24 Accordingly, the purpose of this investigation was to evaluate sex differences in cardiac function after an ultraendurance running race. A secondary purpose was to evaluate the relationship between training experience and acute cardiac responses to PSE. Based on the observations of our previous work, we hypothesized that men would display greater evidence of exerciseinduced cardiac fatigue compared with women. Despite the uncertainty of myocardial fibrosis in previous reports of veteran endurance athletes, global cardiac function remains intact or enhanced compared with age-matched controls,15 thus, we further hypothesized that training experience would not differentiate the magnitude of cardiac fatigue.
METHODS Participants and Ethical Approval
Thirty-four competitors (43.4 6 8.2 years; 13 female) participating in a mountain trail running ultramarathon (Fat Dog 100) volunteered to participate in this research. This field study occurred mid-summer in British Columbia, Canada. Runners were exposed to temperature fluctuations ranging from 6 to 308C between day and night-time hours. The terrain was very mountainous with ascents of 600-2300 m over 2 race distances (100 km and 160 km). Before testing, all participants provided written informed consent in exact accordance with guidelines of the Clinical Research Ethics Review Board at the University of British Columbia.
Protocol Baseline testing occurred at least 1 day before the start of the race in dedicated research space on site (temperature and humidity controlled). Participants completed a training history questionnaire for the determination of training volume and race experience. Assessments included basic anthropometrics, Copyright © 2014 Wolters Kluwer Health, Inc. All rights reserved.
Cardiac Sex Differences and PSE
arterial compliance, BRS, and echocardiography. Immediately after race cessation, runners were met at the finish line. After 5 minutes of seated rest, seated blood pressure (BP) and postrace body mass were measured. Participants were then shuttled in a research vehicle to the testing facility approximately 800 m away, approximately a 2-minute to 3-minute drive, for the vascular assessment. The initiation of postrace assessments typically occurred 20 to 30 minutes from crossing the finish line, beginning with vascular assessments. Echocardiography commenced typically 30 to 40 minutes postexercise. Racers were required to complete a minimum distance of 50 km to be eligible for postrace testing.
Anthropometrics, Autonomic, and Arterial Compliance Assessments Participants were assessed for body height, mass, seated BP, and HR. Postrace body mass, BP, and HR were collected at the finish line. At the research facility, assessments commenced after 5 minutes of supine rest. Five minutes of continuous BP data was collected using finger photoplethysmography (Finapres; Ohmeda, Inc, Englewood, Colorado), calibrated using an automated BP device (Bp-TRU 100; Coquitlam, British Columbia, Canada) along with an electrocardiogram (ECG), synchronized with Powerlab (ADIntruments, Colorado Springs, Colorado) and Chart software (Version 5.5.6). Participants remained supine while wearing industrial strength ear protectors to eliminate any noise-induced oscillations in BRS for 5 minutes of collection. Off-line power spectral evaluations of BRS were conducted by the same investigator using Nevrokard BRS software (Version 6.1.0, Nevrokard, Slovenia) as described previously.25 Arterial compliance was measured noninvasively through applanation tonometry with the HDI CR-2000 (Hypertension Diagnostics, Eagan, Minnesota) for diastolic pulse contour analysis. The calculations of small and large arterial compliance are derived through a paradigm that divides total systemic resistance into individual components using mathematical modeling and has been validated with invasive and noninvasive testing.26,27 After stabilizing the wrist and maximizing signal strength, radial artery tonometry measurements were collected using the right wrist with the automated sphygmomanometer affixed to the upper left arm. Measurements were taken in duplicate with the average used for analysis.
Echocardiographic Assessments Two-dimensional transthoracic and pulse-Doppler imaging was used to assess LV function using a portable ultrasound system (Vivid i; GE Healthcare) with simultaneous ECG and a 2.5-MHz transducer. Participants were positioned in the left lateral decubitus position for imaging. Cardiac images were acquired by a clinically certified sonographer. Parasternal long axis views were obtained for the assessment of LV dimensions and mass and apical 2-chamber and 4-chamber views were acquired for the assessment of volumes, velocities, and strain. Transmitral Doppler peak flow velocities were measured for early (E) and late (A) diastolic filling, in addition to pulmonary venous flow www.cjsportmed.com |
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velocities and durations. Myocardial tissue velocities were assessed at the mitral annulus at the LV septal (E0 septal), LV lateral (E0 lateral), and right ventricular lateral (E0 RV) walls. Parasternal short axis views, obtained mid-ventricle, were obtained to derive circumferential and radial strain and SR data as described in detail elsewhere.28 Briefly, midventricle was defined as the level of the first appearance of the superior surface of the papillary muscle when imaged down from the mitral valve and imaged at high-frame rates (70-90 frames per second). All measures were obtained over 3 cardiac cycles and averaged in the analysis. Ventricular volumes and diameters were analyzed offline (EchoPAC; GE Healthcare, v. 110.1.1) in accordance with the recommendations of the American Society of Echocardiography29 by a single trained observer. End-diastolic volume (EDV) and end-systolic volume were assessed through Simpson bi-plane method and used to calculate stroke volume, cardiac output (CO), and ejection fraction (EF). Fractional shortening (FS) was calculated from ventricular diameters and expressed as a percent. Wall stress (WS) was determined noninvasively as WS (g/cm2) = 0.334(SBP)(LVESD)/PW(1 + PW)/LVESD, where SBP is systolic blood pressure, LVESD is left ventricular end-systolic diameter, and PW is left ventricular systolic posterior wall thickness.30 Evaluation of E/E0 for both the septal and lateral walls provided an estimate of LV filling pressures.
Statistical Analysis A between-group analysis of variance with repeated measures was used to assess the effect of sex on changes in cardiac function (pre-exercise and postexercise). Linear regression was used to assess the effect of vascular and performance variables on the change in major LV functional measures, adjusted for age and sex. To assess the influence of change in loading conditions with exercise, changes in body mass, HR, race distance completed, SBP, ESP/EDV, and E/A were correlated with delta measures of cardiac function using Pearson correlation. All analyses were performed using SPSS software (version 20.0; SPSS IBM, Chicago, Illinois). Significance for all tests was set a priori at P , 0.05. Results are reported as mean 6 SD.
TABLE 1. Participant Characteristics and Baseline Cardiovascular Measures Variable
Men (n = 17)
Age, y Height, cm Body mass, kg LVM, g LVM/BSA, g/m2 SBP, mm Hg DBP, mm Hg HR, bpm CO, L.min21 LAC, mL/mm Hg10 SAC, mL/mm Hg100 BRS, ms/mm Hg
44.8 177.8 77.6 214.7 109.6 128.4 73.0 63.5 5.14 18.3 9.7 18.5
6 6 6 6 6 6 6 6 6 6 6 6
6.6 6.3 9.3 47.11 22.47 7.9 7.0 7.1 1.21 6.0 3.1 11.6
Women (n = 8)
P
6 6 6 6 6 6 6 6 6 6 6 6
0.758 0.001* 0.001* 0.007* 0.235 0.073 0.230 0.221 0.026* 0.074 0.006* 0.310
45.9 162.7 58.9 160.83 98.47 120.8 69.3 59.6 4.00 14.0 6.0 25.0
10.2 5.1 3.6 30.71 18.04 12.5 7.1 5.2 0.80 3.2 2.1 17.6
*P , 0.05 between men and women. LVM, left ventricular mass; BSA, body surface area; DBP, diastolic blood pressure; LAC, large artery compliance; SAC, small artery compliance.
Participant Performance All 25 individuals met the minimum distance criteria, with an average race distance of 134.9 6 49.7 km, over 28 6 8.9 hours. There were no significant differences between sex for race completion time (29.0 6 8.6 vs 25.9 6 9.7 hours), race pace (4.7 6 1.1 vs 4.8 6 0.7 km/h), or race distance completed (141.8 6 50.4 vs 121.1 6 48.4 km) for men and women, respectively. Our participants who crossed the finish line placed first to 16th for the men (n = 14) and third to 15th for the women (n = 5).
Physiological and Cardiovascular Outcomes
Thirty-four participants completed baseline assessments, whereas 25 individuals (8 female) completed the study (n = 21 of European ethnicity). Participants trained on average 5 6 1 d/wk, running 86 6 35 km/wk. The group averaged 5 6 3.4 years of competing in ultramarathons (range, 1-15 years). Total number of lifetime ultramarathons averaged 14.2 6 12.6 (range, 1-53), with the last reported event occurring 51.5 6 51.9 days before this event. Runners reported an average taper of 14 6 11 days and 9.7 6 9.5 days since their last training session. Eighty-four percent of the participants reported ingesting sodium supplements during the race and regularly in training. Participant characteristics and baseline cardiovascular measures are found in Table 1.
From prerace testing, body weight decreased an average of 1.5 6 3.1 kg (P = 0.02). At the finish line, BP and HR responses did not differ by sex. Seated BP was not significantly reduced after race: SBP, 116.2 6 12.9 to 114.2 6 14.2 mm Hg and diastolic blood pressure, 76.5 6 7.2 to 76.1 6 11.0 mm Hg, prerace to postrace, respectively. Heart rate at the finish line was significantly higher than observed prerace (postrace, 89.6 6 13.7 vs prerace, 62.3 6 8.2 bpm; P , 0.001). Assessed at the research station, cardiac dimensions and volumes were altered postexercise, whereas EF and CO were not significantly different (Table 2). Reductions in BRS after exercise did not differ between men and women (Figure 1). Ultraendurance exercise resulted in significant reductions in FS (P = 0.001; Table 2), E/A (P = 0.006), isovolumetric relaxation time (P = 0.045), and peak atrial reverse pulmonary artery flow velocity duration (P = 0.030; Table 3). Septal and lateral tissue velocities and longitudinal strain were also significantly reduced postexercise (P , 0.05; Table 4). Sex differences were found for baseline cardiac structure and global function where men displayed larger LV diameters and volumes, CO, and lower total peripheral resistance (P , 0.05; Table 2). Peak late transmitral flow velocity (Table 3) and estimates of LV filling pressures (E/E0 ) were significantly greater in women compared with men (P , 0.05; Table 4).
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RESULTS Participant Characteristics
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Cardiac Sex Differences and PSE
TABLE 2. Cardiac Dimensions and Global Systolic Function After PSE Pre-exercise Variable LVPWd, cm LVIVSd, cm LVEDD, cm LVPWs, cm* LVIVSs, cm* LVESD, cm LVEDV, mL* LVESV, mL* SV, mL* SVI, mL/m2 EF, % CO, L.min21* CI, L.min21/m2 FS, % SBP/ESV* TPR, mm Hg/L$min21* WS, ·103 dyn/cm2*
Men 0.98 1.3 4.81 1.74 1.88 2.86 138.4 46.7 91.7 46.9 66.4 5.19 2.65 40.9 2.91 18.6 67.7
6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6
Postexercise Women
0.18 0.20 0.35 0.18 0.16 0.41 25.1 13.0 16.0 7.8 5.2 1.19 0.55 6.4 0.69 5.0 4.0
0.89 1.2 4.41 1.53 1.61 2.54 100.9 34.0 66.9 41.2 66.4 4.01 2.47 42.5 3.89 22.6 67.3
6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6
0.25 0.16 0.43 0.26 0.23 0.39 7.1 8.9 8.4 6.3 8.3 0.80 0.55 6.5 1.60 6.3 7.0
Men 1.1 1.4 4.44 1.74 1.84 2.91 111.5 40.1 71.4 36.9 63.8 5.16 2.65 34.1 3.17 17.7 64.0
6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6
Women
0.27 0.30 0.52 0.28 0.24 0.33 16.0† 10.2† 14.7† 8.9† 7.8 1.31 0.68 7.6† 0.72 5.2 5.9
0.95 1.2 4.21 1.39 1.50 2.75 87.8 30.4 57.4 35.2 65.5 4.24 2.60 34.6 4.40 20.2 67.0
6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6
0.18 0.13 0.33 0.25 0.22 0.32 11.1† 11.2† 12.0† 7.1† 11.6 1.09 0.66 7.9† 2.09 4.7 4.8
*P , 0.05 between men and women. †P , 0.05 from pre-exercise. PWd, posterior wall in diastole; IVSd, intraventricular septum in diastole; EDD, end-diastolic diameter; PWs, posterior wall in systole; IVSs, intraventricular septum in systole; ESD, end-systolic diameter; ESV, end-systolic volume; SV, stroke volume; SVI, stroke volume index; CI, cardiac index; TPR, total peripheral resistance.
Pearson correlation analysis revealed that changes in body mass, HR, race distance completed, SBP, ESP/EDV, and E/A were not associated with the reductions in tissue velocities or longitudinal strain. Linear regression analysis adjusted for age and sex for all models determined that baseline large artery compliance was significantly associated with the change in E septal (Std b = 0.507; r2 = 0.237; P = 0.04) and E lateral (Std b = 0.571; r2 = 0.326; P = 0.017) tissue velocities, and change in longitudinal strain (Std b = 0.623; r2 = 0.458; P = 0.003). Thus, participants with higher baseline arterial compliance experienced lower reductions in cardiac function postexercise (Figure 2). Greater lifetime ultramarathons and faster race pace were associated with lower reductions longitudinal strain (Std
FIGURE 1. No sex differences for the change in baroreceptor sensitivity with prolonged exercise. *P , 0.001 from preexercise. Copyright © 2014 Wolters Kluwer Health, Inc. All rights reserved.
b = 0.445; r2 = 0.365; P = 0.019 and Std b = 0.448; r2 = 0.362; P = 0.020, respectively).
DISCUSSION We aimed to compare the cardiovascular response following PSE between men and women. The major findings of this investigation are that (1) men and women displayed similar indications of exercise-induced cardiac fatigue after an ultramarathon, (2) a reduced magnitude of cardiac fatigue as evidenced by LV tissue velocities and strain was associated with higher baseline arterial compliance, and (3) indications of ultraendurance training status and performance suggest less experienced runners are more susceptible to exercise-induced cardiac fatigue than experienced participants. Contrary to our hypothesis, we did not find sex to influence the cardiac response to an ultramarathon. To the best of our knowledge, only an earlier investigation from our laboratory had the objective of comparing sex differences in the acute response to ultraendurance exercise and found sex differences in contractility in triathletes.17 Other laboratorybased investigations of PSE31,32 involved similar samples of men and women to this and our previous work, however, they did not report any sex differentiation other than prerace characteristics. The lack of agreement between the present findings and our previous investigation may potentially be explained by differences in exercise intensity (estimated from running pace to be 80% vs 50% of maximum capacity) and duration (6 vs 29 hours) for the half-ironman triathlon and ultramarathon, respectively. The varied intensities and competitive situations within the literature make isolating any dose–response difficult,1 however, we suspect intensity may www.cjsportmed.com |
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TABLE 3. Doppler Flow Velocities After PSE Pre-exercise Variable E, m/s A, m/s* E/A DecT, ms IVRT, ms S, m/s D, m/s S/D Ar, m/s Ar duration, ms
Men 0.81 0.53 1.28 216.9 84.4 0.56 0.50 1.02 0.24 142.8
6 6 6 6 6 6 6 6 6 6
Postexercise Women
0.20 0.10 0.68 40.4 14.9 0.12 0.13 0.46 0.03 34.5
0.84 0.57 1.55 206.0 89.8 0.52 0.47 1.13 0.25 133.4
6 6 6 6 6 6 6 6 6 6
Men
0.18 0.13 0.51 35.7 11.7 0.08 0.11 0.13 0.04 25.9
0.68 0.55 1.26 206.4 83.1 0.51 0.43 1.17 0.24 123.5
6 6 6 6 6 6 6 6 6 6
Women
0.13 0.11 0.33† 38.7 10.4† 0.17 0.07 0.28 0.05 29.3†
0.84 0.67 1.30 189.9 73.5 0.50 0.47 1.05 0.26 119.6
6 6 6 6 6 6 6 6 6 6
0.08 0.12 0.27† 22.2 19.4† 0.15 0.08 0.21 0.04 12.0†
*P , 0.05 between men and women. †From pre-exercise. E, peak early transmitral flow velocity; A, peak late transmitral flow velocity; DecT, E wave deceleration time; IVRT, isovolumetric relaxation time; S, peak systolic pulmonary venous flow velocity; D, peak diastolic pulmonary venous flow velocity; Ar, peak atrial reverse pulmonary artery flow velocity.
be a key factor as we have found sex differences after a 44minute high-intensity interval cycle exercise.33 Despite the lack of interactions between exerciseinduced cardiac fatigue and sex, we showed evidence of systolic and diastolic impairment, in agreement with previous findings in ultramarathons28,34,35 and other forms of prolonged exercise.32,36,37 Decrements in systolic function as indicated by postexercise reductions of longitudinal strain, myocardial wall velocities, and FS were unrelated to a change in loading conditions (HR, and indirect measures of preload and postload) providing evidence of intrinsic decrements in myocardial performance. As such, the reductions in peak early
transmitral flow velocity and pulmonary vein atrial reverse flow duration are evidence of impaired LV relaxation.37 A novel finding in our work is the strong association of large artery compliance to altered ventricular function when adjusting for age and sex. It is well established that the interaction of the LV with the arterial system is a central determinant of cardiovascular performance and cardiac energetics.38 Furthermore, age-related decreases in LV systolic performance during exercise are associated with suboptimal ventricular–vascular coupling, the extent of which may differ between men and women.39 Thus, enhanced resting arterial compliance would support LV function during
TABLE 4. Tissue Velocities and LV Strain After PSE Pre-exercise Variable Tissue velocities E0 septal, m/s E/E0 septal† E0 lateral, m/s E/E0 lateral† E0 RV, m/s Strain/strain rate Longitudinal S, % Longitudinal SRsys, s21 Longitudinal SRdia, s21 Circumferential S, % Circumferential SRsys, s21 Circumferential SRdia, s21 Radial S, % Radial SRsys, s21 Radial SRdia, s21
Men
Postexercise Women
Men
Women
0.13 5.10 0.17 3.91 0.15
6 6 6 6 6
0.03 3.25 0.03 2.10 0.03
0.12 7.24 0.16 5.63 0.15
6 6 6 6 6
0.03 1.81 0.04 1.98 0.03
0.11 5.96 0.15 4.64 0.15
6 6 6 6 6
0.02* 1.03 0.04* 0.89 0.03
0.11 8.24 0.15 5.67 0.14
6 6 6 6 6
0.02* 2.02 0.04* 1.27 0.03
221.02 21.05 1.37 217.64 21.06 1.16 21.87 1.77 22.04
6 6 6 6 6 6 6 6 6
1.98 0.13 0.24 5.02 0.31 0.49 1.15 0.44 0.50
220.28 21.00 1.47 218.39 21.04 1.32 24.06 1.61 21.88
6 6 6 6 6 6 6 6 6
1.90 0.11 0.24 5.24 0.32 0.58 4.02 0.46 0.72
218.44 21.08 1.29 217.69 21.25 1.15 24.57 1.94 22.06
6 6 6 6 6 6 6 6 6
0.34* 0.18 0.30 4.95 0.33 0.43 4.95 0.46 0.67
218.44 21.02 1.52 218.49 21.10 1.44 22.10 1.84 22.38
6 6 6 6 6 6 6 6 6
2.34* 0.22 0.31 4.59 0.25 0.56 1.52 0.51 0.50
*From pre-exercise. †P , 0.05 between men and women. E0 , myocardial tissue velocity; E, peak early transmitral flow velocity; RV, right ventricle; S, strain; sys, systolic; dia, diastolic.
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FIGURE 2. Association between resting arterial compliance and percent change in LV septal wall tissue velocities (A), LV lateral wall tissue velocities (B), and longitudinal strain (C) after PSE. Dark circles indicate men; open circles, women.
strenuous exercise, as is indicated by lower relative decrements in LV strain and tissue velocities postexercise. Improved arterial compliance and subsequent LV performance may be linked to training status. Endurance training increases arterial compliance and has also been shown to attenuate age-related declines in large artery compliance.40 Further evidence of training status in our cohort may be inferred from measures of race pace and lifetime ultramarathons to represent aspects of aerobic capacity and chronic training, respectively. Cardiac output and perfusion pressure are compromised in untrained individuals when both the metabolic and thermoregulatory demands are high.41 In a meta-analysis reviewing LV function with ultraendurance exercise, one of the factors influencing a decline in systolic function was poor training status.7 Thus, our findings suggest that greater training experience, and subsequent improvements in fitness, may Copyright © 2014 Wolters Kluwer Health, Inc. All rights reserved.
Cardiac Sex Differences and PSE
reduce the cardiovascular strain that may accompany ultraendurance exercise. However, recent reports of myocardial fibrosis in veteran endurance athletes,15,42,43 linked to years of training competing,15 do not support our speculation. The efficacy and potential risks of long-term endurance training remain in question.10 Interestingly, although not all investigations have found evidence of exercise-induced cardiac fatigue after PSE, there have been reports of reduced radial, circumferential and longitudinal strain, and SRs in ultra-events.28,36 In the present investigation, reductions in LV tissue velocities and longitudinal strain did not extend to the radial and circumferential planes. Ventricular dysfunction has been suggested to begin in the longitudinal plane while circumferential and radial compensations remain to preserve EF under stress.44 Thus, in the present investigation, cardiac fatigue may be described as moderate in comparison with events of similar magnitude.28,36 Because exercise duration may be associated with exercise-induced cardiac fatigue,5,6,45 it was expected that this ultramarathon occurring in an extreme mountain terrain environment would have induced greater impairments in ventricular function. Temperature and intensity may be contributing factors. In the Western States Endurance Race,28 racers presumably had much higher thermal strain to contend with than our temperate mountain race. Heat stress translocates blood volume from the centre to the periphery, for which the demand for skin blood flow is met in part by an increase in CO.46 However, over the course of the ultramarathon, competing demands for blood flow between working musculature and skin perfusion and may alter the myocardial perfusion-towork relationship, leading to impaired myocardial function.41 Alternatively, the extreme mountainous terrain of the Fat Dog 100 may have induced considerable neuromuscular fatigue47 and as a result lowered exercise intensity enough to spare cardiovascular fatigue. Mattsson et al48 recently showed that when exercise duration exceeds 24 hours, cardiac work (stroke work · HR) and myocardial oxygen consumption decrease, likely as a physiological adaptation to maintain CO when total energy expenditure demands are high. The relative contribution of these factors on LV function with PSE requires further research. A limitation of this investigation is the small sample of female subjects relative to the males. Recruitment of participants in field studies is limited to those runners who wish to participate. Because ultraendurance competitors are typically only 20% female,16 it becomes increasingly difficult to study females in numbers relative to males. After attrition, females represented 32% of our cohort, which is in proportion to the female racers participating in the event. Posteriori calculations revealed a moderate effect size consistent across most variables (h = 0.28-0.67). Interestingly, we have previously reported sex differences following laboratory-based investigations of strenuous exercise using similar sample sizes,17,33 thus, we do not believe this factor impacted our results, although we cannot exclude the possibility of a type II error. In concert with the same recruitment issues, it is also not possible to recruit based on fitness. Our sample included the first place finisher completing the race in 28 hours with our last finisher coming in at 41 hours. Because logistical issues limited the assessment of www.cjsportmed.com |
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each participant’s aerobic capacity, we are unable to determine whether the men and women were equal with respect to relative V̇ O2max. Nonetheless, we are confident in our use of race pace and race time as surrogate measures of fitness status, and such practice has been reported by others.49 Another consideration is the prevalence of sodium supplementation in our sample of ultramarathoners. In this study, we were unable to control for the form, quantity, and frequency of sodium ingested. Sodium loading has been shown to increase plasma volume at rest and reduce physiological strain in warm conditions, significantly improving exercise capacity.50 How sodium affects exercise-induced cardiac fatigue is not known and should be the focus of future investigations exploring exercise-induced cardiac fatigue. The results of this investigation suggest that in response to an acute bout of PSE, cardiac adjustments are similar in men and women. Independent of sex, we present indications for reduced cardiovascular strain associated with indices of enhanced vascular health and greater training experience. Considering recent clinical concerns pertaining to the effects of PSE on the heart, further research is required to delineate the impact of acute and chronic exposure to PSE on LV function and long-term cardiac health.
1. Dawson E, George K, Shave R, et al. Does the human heart fatigue subsequent to prolonged exercise? Sports Med. 2003;33:365–380. 2. Middleton N, Shave R, George K, et al. Novel application of flow propagation velocity and ischaemia-modified albumin in analysis of postexercise cardiac function in man. Exp Physiol. 2006;91:511–519. 3. Seals DR, Rogers MA, Hagberg JM, et al. Left ventricular dysfunction after prolonged strenuous exercise in healthy subjects. Am J Cardiol. 1988;61:875–879. 4. Douglas PS, O’Toole ML, Hiller WD, et al. Cardiac fatigue after prolonged exercise. Circulation. 1987;76:1206–1213. 5. McGavock JM, Warburton DE, Taylor D, et al. The effects of prolonged strenuous exercise on left ventricular function: a brief review. Heart Lung. 2002;31:279–292; quiz 274–293. 6. Whyte GP, George K, Sharma S, et al. Cardiac fatigue following prolonged endurance exercise of differing distances. Med Sci Sports Exerc. 2000;32:1067–1072. 7. Middleton N, Shave R, George K, et al. Left ventricular function immediately following prolonged exercise: a meta-analysis. Med Sci Sports Exerc. 2006;38:681–687. 8. Scott JM, Warburton DE. Mechanisms underpinning exercise-induced changes in left ventricular function. Med Sci Sports Exerc. 2008;40: 1400–1407. 9. Oxborough D, Birch K, Shave R, et al. “Exercise-induced cardiac fatigue”—a review of the echocardiographic literature. Echocardiography. 2010;27:1130–1140. 10. George K, Spence A, Naylor LH, et al. Cardiac adaptation to acute and chronic participation in endurance sports. Heart. 2011;97:1999–2004. 11. Knechtle B, Knechtle P, Lepers R. Participation and performance trends in ultra-triathlons from 1985 to 2009. Scand J Med Sci Sports. 2011;21: e82–e90. 12. Hoffman MD. Performance trends in 161-km ultramarathons. Int J Sports Med. 2010;31:31–37. 13. Yared K, Wood MJ. Is marathon running hazardous to your cardiovascular health? The jury is still out. Radiology. 2009;251:3–5.
14. O’Keefe JH, Patil HR, Lavie CJ, et al. Potential adverse cardiovascular effects from excessive endurance exercise. Mayo Clin Proc. 2012;87: 587–595. 15. Wilson M, O’Hanlon R, Prasad S, et al. Diverse patterns of myocardial fibrosis in lifelong, veteran endurance athletes. J Appl Physiol. 2011;110: 1622–1626. 16. Hoffman MD, Ong JC, Wang G. Historical analysis of participation in 161 km ultramarathons in North America. Int J Hist Sport. 2010;27: 1877–1891. 17. Scott JM, Esch BT, Haykowsky MJ, et al. Sex differences in left ventricular function and beta-receptor responsiveness following prolonged strenuous exercise. J Appl Physiol. 2007;102:681–687. 18. Ohba H, Takada H, Musha H, et al. Effects of prolonged strenuous exercise on plasma levels of atrial natriuretic peptide and brain natriuretic peptide in healthy men. Am Heart J. 2001;141:751–758. 19. Schroeder C, Adams F, Boschmann M, et al. Phenotypical evidence for a gender difference in cardiac norepinephrine transporter function. Am J Physiol Regul Integr Comp Physiol. 2004;286:R851–R856. 20. Ramaekers D, Ector H, Aubert AE, et al. Heart rate variability and heart rate in healthy volunteers. Is the female autonomic nervous system cardioprotective? Eur Heart J. 1998;19:1334–1341. 21. Hautala AJ, Makikallio TH, Seppanen T, et al. Short-term correlation properties of R-R interval dynamics at different exercise intensity levels. Clin Physiol Funct Imaging. 2003;23:215–223. 22. Mendonca GV, Heffernan KS, Rossow L, et al. Sex differences in linear and nonlinear heart rate variability during early recovery from supramaximal exercise. Appl Physiol Nutr Metab. 2010;35:439–446. 23. Shave R, George K, Whyte G, et al. A comparison of Doppler, tissue Doppler imaging, and strain rate imaging in the assessment of postexercise left ventricular function. Appl Physiol Nutr Metab. 2009;34:33–39. 24. La Rovere MT, Pinna GD, Raczak G. Baroreflex sensitivity: measurement and clinical implications. Ann Noninvasive Electrocardiol. 2008; 13:191–207. 25. Cote AT, Bredin SS, Phillips AA, et al. Predictors of orthostatic intolerance in healthy young women. Clin Invest Med. 2012;35:E65–E74. 26. Cohn JN, Finkelstein S, McVeigh G, et al. Noninvasive pulse wave analysis for the early detection of vascular disease. Hypertension. 1995;26:503–508. 27. Resnick LM, Militianu D, Cunnings AJ, et al. Pulse waveform analysis of arterial compliance: relation to other techniques, age, and metabolic variables. Am J Hypertens. 2000;13:1243–1249. 28. Scott JM, Esch BT, Shave R, et al. Cardiovascular consequences of completing a 160-km ultramarathon. Med Sci Sports Exerc. 2009;41: 26–34. 29. Lang RM, Bierig M, Devereux RB, et al. Recommendations for chamber quantification: a report from the American Society of Echocardiography’s Guidelines and Standards Committee and the Chamber Quantification Writing Group, developed in conjunction with the European Association of Echocardiography, a branch of the European Society of Cardiology. J Am Soc Echocardiogr. 2005;18:1440–1463. 30. Reichek N, Wilson J, St John Sutton M, et al. Noninvasive determination of left ventricular end-systolic stress: validation of the method and initial application. Circulation. 1982;65:99–108. 31. Banks L, Sasson Z, Busato M, et al. Impaired left and right ventricular function following prolonged exercise in young athletes: influence of exercise intensity and responses to dobutamine stress. J Appl Physiol. 2010;108:112–119. 32. La Gerche A, Connelly KA, Mooney DJ, et al. Biochemical and functional abnormalities of left and right ventricular function after ultraendurance exercise. Heart. 2008;94:860–866. 33. Cote AT, Bredin SS, Phillips AA, et al. Left ventricular mechanics and arterial-ventricular coupling following high-intensity interval exercise. J Appl Physiol (1985). 2013;115:1705–1713. 34. Niemela KO, Palatsi IJ, Ikaheimo MJ, et al. Evidence of impaired left ventricular performance after an uninterrupted competitive 24 hour run. Circulation. 1984;70:350–356. 35. Niemela K, Palatsi I, Ikaheimo M, et al. Impaired left ventricular diastolic function in athletes after utterly strenuous prolonged exercise. Int J Sports Med. 1987;8:61–65. 36. Nottin S, Doucende G, Schuster I, et al. Alteration in left ventricular strains and torsional mechanics after ultralong duration exercise in athletes. Circ Cardiovasc Imaging. 2009;2:323–330.
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ACKNOWLEDGMENTS The authors acknowledge Dr. Jack Taunton and GE Healthcare for their technical expertise in this project. REFERENCES
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Clin J Sport Med Volume 25, Number 3, May 2015 37. George K, Oxborough D, Forster J, et al. Mitral annular myocardial velocity assessment of segmental left ventricular diastolic function after prolonged exercise in humans. J Physiol. 2005;569:305–313. 38. Chantler PD, Lakatta EG, Najjar SS. Arterial-ventricular coupling: mechanistic insights into cardiovascular performance at rest and during exercise. J Appl Physiol. 2008;105:1342–1351. 39. Najjar SS, Schulman SP, Gerstenblith G, et al. Age and gender affect ventricular-vascular coupling during aerobic exercise. J Am Coll Cardiol. 2004;44:611–617. 40. Seals DR. Habitual exercise and the age-associated decline in large artery compliance. Exerc Sport Sci Rev. 2003;31:68–72. 41. Crandall CG, Gonzalez-Alonso J. Cardiovascular function in the heatstressed human. Acta Physiol (Oxf). 2010;199:407–423. 42. Lindsay MM, Dunn FG. Biochemical evidence of myocardial fibrosis in veteran endurance athletes. Br J Sports Med. 2007;41:447–452. 43. Whyte G, Sheppard M, George K, et al. Post-mortem evidence of idiopathic left ventricular hypertrophy and idiopathic interstitial myocardial fibrosis: is exercise the cause? Br J Sports Med. 2008;42:304–305. 44. Mizuguchi Y, Oishi Y, Miyoshi H, et al. The functional role of longitudinal, circumferential, and radial myocardial deformation for regulating
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45. 46. 47. 48. 49. 50.
the early impairment of left ventricular contraction and relaxation in patients with cardiovascular risk factors: a study with two-dimensional strain imaging. J Am Soc Echocardiogr. 2008;21:1138–1144. Shave RE, Dawson E, Whyte G, et al. Evidence of exercise-induced cardiac dysfunction and elevated cTnT in separate cohorts competing in an ultraendurance mountain marathon race. Int J Sports Med. 2002;23:489–494. Crandall CG, Wilson TE, Marving J, et al. Effects of passive heating on central blood volume and ventricular dimensions in humans. J Physiol. 2008;586:293–301. Millet GY, Tomazin K, Verges S, et al. Neuromuscular consequences of an extreme mountain ultra-marathon. PLoS One. 2011;6:e17059. Mattsson CM, Stahlberg M, Larsen FJ, et al. Late cardiovascular drift observable during ultraendurance exercise. Med Sci Sports Exerc. 2011; 43:1162–1168. George K, Whyte G, Stephenson C, et al. Postexercise left ventricular function and cTnT in recreational marathon runners. Med Sci Sports Exerc. 2004;36:1709–1715. Sims ST, van Vliet L, Cotter JD, et al. Sodium loading aids fluid balance and reduces physiological strain of trained men exercising in the heat. Med Sci Sports Exerc. 2007;39:123–130.
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Sex Differences in Cardiac Function After Prolonged Strenuous Exercise Anita T. Cote, PhD,* Aaron A. Phillips, PhD,*† Heather J. Foulds, MSc,*† Sarah A. Charlesworth, PhD,* Shannon S.D. Bredin, PhD,* Jamie F. Burr, PhD,‡ Michael S. Koehle, MD, PhD,§¶ and Darren E.R. Warburton, PhD*†
Objective: To evaluate sex differences in left ventricular (LV) function after an ultramarathon, and the association of vascular and training indices with the magnitude of exercise-induced cardiac fatigue.
Design: Descriptive field study. Setting: Fat Dog 100 Ultramarathon Trail Race, Canada. Participants: Thirty-four (13 women) recreational runners (aged
Regression analysis found that higher baseline arterial compliance was associated with lower reductions in cardiac function postexercise, to which sex was a significant factor for E0 of the lateral wall. Faster race pace and greater lifetime ultramarathons were associated with lower reductions in LV longitudinal strain (P , 0.05).
Conclusions: Cardiac responses after an ultramarathon were similar between men and women. Greater evidence of exerciseinduced cardiac fatigue was found to be associated with lower baseline arterial compliance and training status/experience.
28-56 years).
Clinical Relevance: These findings suggest that vascular health is
Interventions: A 100-km or 160-km mountain marathon.
an important contributor to the degree of cardiovascular strain incurred as the result of an acute bout of prolonged strenuous exercise.
Main Outcome Measures: Baseline baroreceptor sensitivity, heart rate variability, and arterial compliance; Pre-exercise and postexercise echocardiographic evaluations of LV dimensions, volumes, Doppler flow velocities, tissue velocities, strain, and strain rate.
Key Words: cardiac fatigue, ultraendurance exercise, echocardiography (Clin J Sport Med 2015;25:276–283)
Results: Finishers represented 17 men (44.8 6 6.6 years) and 8
women (45.9 6 10.2 years; P = 0.758). After ultraendurance exercise, significant reductions (P , 0.05) in fractional shortening (men: 40.9 6 6.9 to 34.1 6 7.6%; women: 42.5 6 6.5 to 34.6 6 7.9%) diastolic filling (E/A, men: 1.28 6 0.68 to 1.26 6 0.33; women: 1.55 6 0.51 to 1.30 6 0.27), septal and lateral tissue velocities (E0 ), and longitudinal strain (men: 221.02 6 1.98 to 218.44 6 0.34; women: 220.28 6 1.90 to 218.44 6 2.34) were observed. Sex differences were found for baseline cardiac structure and global function, peak late transmitral flow velocity, and estimates of LV filling pressures (P , 0.05). Submitted for publication September 11, 2013; accepted March 18, 2014. From the *Cardiovascular Physiology and Rehabilitation Laboratory, University of British Columbia, Vancouver, Canada; †Experimental Medicine Program, Faculty of Medicine, University of British Columbia, Vancouver, Canada; ‡Applied Human Sciences, University of Prince Edward Island, Charlottetown, Canada; §Environmental Physiology Laboratory, School of Kinesiology, University of British Columbia, Vancouver, Canada; and ¶Division of Sports Medicine, University of British Columbia, Vancouver, Canada. Supported by the Canadian Institutes of Health Research, Michael Smith Foundation for Health Research, Canada Foundation for Innovation, National Science and Engineering Research Council, and the British Columbia Knowledge & Development Fund. D. E. R. Warburton was supported by salary awards from the Canadian Institutes of Health Research and the Michael Smith Foundation for Health Research. All authors report no conflicts of interest. Corresponding Author: Darren E.R. Warburton, PhD, Unit II Osborne Centre, 6108 Thunderbird Blvd, University of British Columbia, Vancouver, BC V6T 1Z3, Canada ([email protected]). Copyright © 2014 Wolters Kluwer Health, Inc. All rights reserved.
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INTRODUCTION Exercise-induced cardiac fatigue is characterized by a reduction in left ventricular (LV) systolic and diastolic function subsequent to exercise in healthy humans,1 particularly prolonged strenuous exercise (PSE).2 These reductions in LV performance have been found to occur despite the absence of underlying cardiovascular pathologies3–6 and seem to be transient in nature with normal function restored typically within 48 hours7 However, the clinical relevance of exercise-induced cardiac fatigue warrants further study,8–10 particularly considering the appreciable increase in ultraendurance participation over recent years.11 The average age of winning ultramarathoners is older than the typical age of winning marathoners.12 This may be interpreted that to perform well in ultraendurance events, accumulating greater years of training may be beneficial, although the cumulative effects of chronic PSE on the cardiovascular system is unclear.13 The juxtaposition of low mortality rates and excellent functional capacity in lifelong exercisers, alongside reports of adverse structural and electrical cardiac remodeling,14,15 brings into question the risks involved with lifelong, high-volume endurance training. Another emerging trend is the increase in female participants in ultraendurance events where female finishers increased 20% in a 4-year span.16 Despite this increase in female competitors, the literature to date has yielded limited Clin J Sport Med Volume 25, Number 3, May 2015
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Clin J Sport Med Volume 25, Number 3, May 2015
information regarding the cardiovascular consequences of PSE in women. Previous work from our research group found males experienced greater reductions in LV systolic function as a consequence of a half-ironman triathlon compared with female competitors,17 the mechanisms of which are not known. Prolonged strenuous exercise has been shown to significantly increase plasma catecholamines,18 a marker of sympathetic activity. Phenotypical evidence of sex differences in cardiac norepinephrine transporter function19 suggests that males exhibit differences in cardiac-specific sympathetic activity. Although, women typically display greater parasympathetic control of heart rate (HR) than men at rest, considered to be a reflection of the enhanced cardioprotection characteristic of healthy pre-menopausal females,20 sympathovagal balance of women may be more vulnerable to the effects of strenuous exercise than men.21,22 Thus, how sex may influence the cardiac responses to significant physiological stress, such as PSE, is not clear. As a means to address this question, assessment of regional myocardial function, such as strain and strain rate (SR) imaging, will provide a thorough analysis of LV function.23 In addition, spontaneous measures of cardiovagal baroreflex sensitivity (BRS) can provide a noninvasive indication of autonomic modulation with exercise.24 Accordingly, the purpose of this investigation was to evaluate sex differences in cardiac function after an ultraendurance running race. A secondary purpose was to evaluate the relationship between training experience and acute cardiac responses to PSE. Based on the observations of our previous work, we hypothesized that men would display greater evidence of exerciseinduced cardiac fatigue compared with women. Despite the uncertainty of myocardial fibrosis in previous reports of veteran endurance athletes, global cardiac function remains intact or enhanced compared with age-matched controls,15 thus, we further hypothesized that training experience would not differentiate the magnitude of cardiac fatigue.
METHODS Participants and Ethical Approval
Thirty-four competitors (43.4 6 8.2 years; 13 female) participating in a mountain trail running ultramarathon (Fat Dog 100) volunteered to participate in this research. This field study occurred mid-summer in British Columbia, Canada. Runners were exposed to temperature fluctuations ranging from 6 to 308C between day and night-time hours. The terrain was very mountainous with ascents of 600-2300 m over 2 race distances (100 km and 160 km). Before testing, all participants provided written informed consent in exact accordance with guidelines of the Clinical Research Ethics Review Board at the University of British Columbia.
Protocol Baseline testing occurred at least 1 day before the start of the race in dedicated research space on site (temperature and humidity controlled). Participants completed a training history questionnaire for the determination of training volume and race experience. Assessments included basic anthropometrics, Copyright © 2014 Wolters Kluwer Health, Inc. All rights reserved.
Cardiac Sex Differences and PSE
arterial compliance, BRS, and echocardiography. Immediately after race cessation, runners were met at the finish line. After 5 minutes of seated rest, seated blood pressure (BP) and postrace body mass were measured. Participants were then shuttled in a research vehicle to the testing facility approximately 800 m away, approximately a 2-minute to 3-minute drive, for the vascular assessment. The initiation of postrace assessments typically occurred 20 to 30 minutes from crossing the finish line, beginning with vascular assessments. Echocardiography commenced typically 30 to 40 minutes postexercise. Racers were required to complete a minimum distance of 50 km to be eligible for postrace testing.
Anthropometrics, Autonomic, and Arterial Compliance Assessments Participants were assessed for body height, mass, seated BP, and HR. Postrace body mass, BP, and HR were collected at the finish line. At the research facility, assessments commenced after 5 minutes of supine rest. Five minutes of continuous BP data was collected using finger photoplethysmography (Finapres; Ohmeda, Inc, Englewood, Colorado), calibrated using an automated BP device (Bp-TRU 100; Coquitlam, British Columbia, Canada) along with an electrocardiogram (ECG), synchronized with Powerlab (ADIntruments, Colorado Springs, Colorado) and Chart software (Version 5.5.6). Participants remained supine while wearing industrial strength ear protectors to eliminate any noise-induced oscillations in BRS for 5 minutes of collection. Off-line power spectral evaluations of BRS were conducted by the same investigator using Nevrokard BRS software (Version 6.1.0, Nevrokard, Slovenia) as described previously.25 Arterial compliance was measured noninvasively through applanation tonometry with the HDI CR-2000 (Hypertension Diagnostics, Eagan, Minnesota) for diastolic pulse contour analysis. The calculations of small and large arterial compliance are derived through a paradigm that divides total systemic resistance into individual components using mathematical modeling and has been validated with invasive and noninvasive testing.26,27 After stabilizing the wrist and maximizing signal strength, radial artery tonometry measurements were collected using the right wrist with the automated sphygmomanometer affixed to the upper left arm. Measurements were taken in duplicate with the average used for analysis.
Echocardiographic Assessments Two-dimensional transthoracic and pulse-Doppler imaging was used to assess LV function using a portable ultrasound system (Vivid i; GE Healthcare) with simultaneous ECG and a 2.5-MHz transducer. Participants were positioned in the left lateral decubitus position for imaging. Cardiac images were acquired by a clinically certified sonographer. Parasternal long axis views were obtained for the assessment of LV dimensions and mass and apical 2-chamber and 4-chamber views were acquired for the assessment of volumes, velocities, and strain. Transmitral Doppler peak flow velocities were measured for early (E) and late (A) diastolic filling, in addition to pulmonary venous flow www.cjsportmed.com |
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velocities and durations. Myocardial tissue velocities were assessed at the mitral annulus at the LV septal (E0 septal), LV lateral (E0 lateral), and right ventricular lateral (E0 RV) walls. Parasternal short axis views, obtained mid-ventricle, were obtained to derive circumferential and radial strain and SR data as described in detail elsewhere.28 Briefly, midventricle was defined as the level of the first appearance of the superior surface of the papillary muscle when imaged down from the mitral valve and imaged at high-frame rates (70-90 frames per second). All measures were obtained over 3 cardiac cycles and averaged in the analysis. Ventricular volumes and diameters were analyzed offline (EchoPAC; GE Healthcare, v. 110.1.1) in accordance with the recommendations of the American Society of Echocardiography29 by a single trained observer. End-diastolic volume (EDV) and end-systolic volume were assessed through Simpson bi-plane method and used to calculate stroke volume, cardiac output (CO), and ejection fraction (EF). Fractional shortening (FS) was calculated from ventricular diameters and expressed as a percent. Wall stress (WS) was determined noninvasively as WS (g/cm2) = 0.334(SBP)(LVESD)/PW(1 + PW)/LVESD, where SBP is systolic blood pressure, LVESD is left ventricular end-systolic diameter, and PW is left ventricular systolic posterior wall thickness.30 Evaluation of E/E0 for both the septal and lateral walls provided an estimate of LV filling pressures.
Statistical Analysis A between-group analysis of variance with repeated measures was used to assess the effect of sex on changes in cardiac function (pre-exercise and postexercise). Linear regression was used to assess the effect of vascular and performance variables on the change in major LV functional measures, adjusted for age and sex. To assess the influence of change in loading conditions with exercise, changes in body mass, HR, race distance completed, SBP, ESP/EDV, and E/A were correlated with delta measures of cardiac function using Pearson correlation. All analyses were performed using SPSS software (version 20.0; SPSS IBM, Chicago, Illinois). Significance for all tests was set a priori at P , 0.05. Results are reported as mean 6 SD.
TABLE 1. Participant Characteristics and Baseline Cardiovascular Measures Variable
Men (n = 17)
Age, y Height, cm Body mass, kg LVM, g LVM/BSA, g/m2 SBP, mm Hg DBP, mm Hg HR, bpm CO, L.min21 LAC, mL/mm Hg10 SAC, mL/mm Hg100 BRS, ms/mm Hg
44.8 177.8 77.6 214.7 109.6 128.4 73.0 63.5 5.14 18.3 9.7 18.5
6 6 6 6 6 6 6 6 6 6 6 6
6.6 6.3 9.3 47.11 22.47 7.9 7.0 7.1 1.21 6.0 3.1 11.6
Women (n = 8)
P
6 6 6 6 6 6 6 6 6 6 6 6
0.758 0.001* 0.001* 0.007* 0.235 0.073 0.230 0.221 0.026* 0.074 0.006* 0.310
45.9 162.7 58.9 160.83 98.47 120.8 69.3 59.6 4.00 14.0 6.0 25.0
10.2 5.1 3.6 30.71 18.04 12.5 7.1 5.2 0.80 3.2 2.1 17.6
*P , 0.05 between men and women. LVM, left ventricular mass; BSA, body surface area; DBP, diastolic blood pressure; LAC, large artery compliance; SAC, small artery compliance.
Participant Performance All 25 individuals met the minimum distance criteria, with an average race distance of 134.9 6 49.7 km, over 28 6 8.9 hours. There were no significant differences between sex for race completion time (29.0 6 8.6 vs 25.9 6 9.7 hours), race pace (4.7 6 1.1 vs 4.8 6 0.7 km/h), or race distance completed (141.8 6 50.4 vs 121.1 6 48.4 km) for men and women, respectively. Our participants who crossed the finish line placed first to 16th for the men (n = 14) and third to 15th for the women (n = 5).
Physiological and Cardiovascular Outcomes
Thirty-four participants completed baseline assessments, whereas 25 individuals (8 female) completed the study (n = 21 of European ethnicity). Participants trained on average 5 6 1 d/wk, running 86 6 35 km/wk. The group averaged 5 6 3.4 years of competing in ultramarathons (range, 1-15 years). Total number of lifetime ultramarathons averaged 14.2 6 12.6 (range, 1-53), with the last reported event occurring 51.5 6 51.9 days before this event. Runners reported an average taper of 14 6 11 days and 9.7 6 9.5 days since their last training session. Eighty-four percent of the participants reported ingesting sodium supplements during the race and regularly in training. Participant characteristics and baseline cardiovascular measures are found in Table 1.
From prerace testing, body weight decreased an average of 1.5 6 3.1 kg (P = 0.02). At the finish line, BP and HR responses did not differ by sex. Seated BP was not significantly reduced after race: SBP, 116.2 6 12.9 to 114.2 6 14.2 mm Hg and diastolic blood pressure, 76.5 6 7.2 to 76.1 6 11.0 mm Hg, prerace to postrace, respectively. Heart rate at the finish line was significantly higher than observed prerace (postrace, 89.6 6 13.7 vs prerace, 62.3 6 8.2 bpm; P , 0.001). Assessed at the research station, cardiac dimensions and volumes were altered postexercise, whereas EF and CO were not significantly different (Table 2). Reductions in BRS after exercise did not differ between men and women (Figure 1). Ultraendurance exercise resulted in significant reductions in FS (P = 0.001; Table 2), E/A (P = 0.006), isovolumetric relaxation time (P = 0.045), and peak atrial reverse pulmonary artery flow velocity duration (P = 0.030; Table 3). Septal and lateral tissue velocities and longitudinal strain were also significantly reduced postexercise (P , 0.05; Table 4). Sex differences were found for baseline cardiac structure and global function where men displayed larger LV diameters and volumes, CO, and lower total peripheral resistance (P , 0.05; Table 2). Peak late transmitral flow velocity (Table 3) and estimates of LV filling pressures (E/E0 ) were significantly greater in women compared with men (P , 0.05; Table 4).
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RESULTS Participant Characteristics
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Cardiac Sex Differences and PSE
TABLE 2. Cardiac Dimensions and Global Systolic Function After PSE Pre-exercise Variable LVPWd, cm LVIVSd, cm LVEDD, cm LVPWs, cm* LVIVSs, cm* LVESD, cm LVEDV, mL* LVESV, mL* SV, mL* SVI, mL/m2 EF, % CO, L.min21* CI, L.min21/m2 FS, % SBP/ESV* TPR, mm Hg/L$min21* WS, ·103 dyn/cm2*
Men 0.98 1.3 4.81 1.74 1.88 2.86 138.4 46.7 91.7 46.9 66.4 5.19 2.65 40.9 2.91 18.6 67.7
6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6
Postexercise Women
0.18 0.20 0.35 0.18 0.16 0.41 25.1 13.0 16.0 7.8 5.2 1.19 0.55 6.4 0.69 5.0 4.0
0.89 1.2 4.41 1.53 1.61 2.54 100.9 34.0 66.9 41.2 66.4 4.01 2.47 42.5 3.89 22.6 67.3
6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6
0.25 0.16 0.43 0.26 0.23 0.39 7.1 8.9 8.4 6.3 8.3 0.80 0.55 6.5 1.60 6.3 7.0
Men 1.1 1.4 4.44 1.74 1.84 2.91 111.5 40.1 71.4 36.9 63.8 5.16 2.65 34.1 3.17 17.7 64.0
6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6
Women
0.27 0.30 0.52 0.28 0.24 0.33 16.0† 10.2† 14.7† 8.9† 7.8 1.31 0.68 7.6† 0.72 5.2 5.9
0.95 1.2 4.21 1.39 1.50 2.75 87.8 30.4 57.4 35.2 65.5 4.24 2.60 34.6 4.40 20.2 67.0
6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6
0.18 0.13 0.33 0.25 0.22 0.32 11.1† 11.2† 12.0† 7.1† 11.6 1.09 0.66 7.9† 2.09 4.7 4.8
*P , 0.05 between men and women. †P , 0.05 from pre-exercise. PWd, posterior wall in diastole; IVSd, intraventricular septum in diastole; EDD, end-diastolic diameter; PWs, posterior wall in systole; IVSs, intraventricular septum in systole; ESD, end-systolic diameter; ESV, end-systolic volume; SV, stroke volume; SVI, stroke volume index; CI, cardiac index; TPR, total peripheral resistance.
Pearson correlation analysis revealed that changes in body mass, HR, race distance completed, SBP, ESP/EDV, and E/A were not associated with the reductions in tissue velocities or longitudinal strain. Linear regression analysis adjusted for age and sex for all models determined that baseline large artery compliance was significantly associated with the change in E septal (Std b = 0.507; r2 = 0.237; P = 0.04) and E lateral (Std b = 0.571; r2 = 0.326; P = 0.017) tissue velocities, and change in longitudinal strain (Std b = 0.623; r2 = 0.458; P = 0.003). Thus, participants with higher baseline arterial compliance experienced lower reductions in cardiac function postexercise (Figure 2). Greater lifetime ultramarathons and faster race pace were associated with lower reductions longitudinal strain (Std
FIGURE 1. No sex differences for the change in baroreceptor sensitivity with prolonged exercise. *P , 0.001 from preexercise. Copyright © 2014 Wolters Kluwer Health, Inc. All rights reserved.
b = 0.445; r2 = 0.365; P = 0.019 and Std b = 0.448; r2 = 0.362; P = 0.020, respectively).
DISCUSSION We aimed to compare the cardiovascular response following PSE between men and women. The major findings of this investigation are that (1) men and women displayed similar indications of exercise-induced cardiac fatigue after an ultramarathon, (2) a reduced magnitude of cardiac fatigue as evidenced by LV tissue velocities and strain was associated with higher baseline arterial compliance, and (3) indications of ultraendurance training status and performance suggest less experienced runners are more susceptible to exercise-induced cardiac fatigue than experienced participants. Contrary to our hypothesis, we did not find sex to influence the cardiac response to an ultramarathon. To the best of our knowledge, only an earlier investigation from our laboratory had the objective of comparing sex differences in the acute response to ultraendurance exercise and found sex differences in contractility in triathletes.17 Other laboratorybased investigations of PSE31,32 involved similar samples of men and women to this and our previous work, however, they did not report any sex differentiation other than prerace characteristics. The lack of agreement between the present findings and our previous investigation may potentially be explained by differences in exercise intensity (estimated from running pace to be 80% vs 50% of maximum capacity) and duration (6 vs 29 hours) for the half-ironman triathlon and ultramarathon, respectively. The varied intensities and competitive situations within the literature make isolating any dose–response difficult,1 however, we suspect intensity may www.cjsportmed.com |
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TABLE 3. Doppler Flow Velocities After PSE Pre-exercise Variable E, m/s A, m/s* E/A DecT, ms IVRT, ms S, m/s D, m/s S/D Ar, m/s Ar duration, ms
Men 0.81 0.53 1.28 216.9 84.4 0.56 0.50 1.02 0.24 142.8
6 6 6 6 6 6 6 6 6 6
Postexercise Women
0.20 0.10 0.68 40.4 14.9 0.12 0.13 0.46 0.03 34.5
0.84 0.57 1.55 206.0 89.8 0.52 0.47 1.13 0.25 133.4
6 6 6 6 6 6 6 6 6 6
Men
0.18 0.13 0.51 35.7 11.7 0.08 0.11 0.13 0.04 25.9
0.68 0.55 1.26 206.4 83.1 0.51 0.43 1.17 0.24 123.5
6 6 6 6 6 6 6 6 6 6
Women
0.13 0.11 0.33† 38.7 10.4† 0.17 0.07 0.28 0.05 29.3†
0.84 0.67 1.30 189.9 73.5 0.50 0.47 1.05 0.26 119.6
6 6 6 6 6 6 6 6 6 6
0.08 0.12 0.27† 22.2 19.4† 0.15 0.08 0.21 0.04 12.0†
*P , 0.05 between men and women. †From pre-exercise. E, peak early transmitral flow velocity; A, peak late transmitral flow velocity; DecT, E wave deceleration time; IVRT, isovolumetric relaxation time; S, peak systolic pulmonary venous flow velocity; D, peak diastolic pulmonary venous flow velocity; Ar, peak atrial reverse pulmonary artery flow velocity.
be a key factor as we have found sex differences after a 44minute high-intensity interval cycle exercise.33 Despite the lack of interactions between exerciseinduced cardiac fatigue and sex, we showed evidence of systolic and diastolic impairment, in agreement with previous findings in ultramarathons28,34,35 and other forms of prolonged exercise.32,36,37 Decrements in systolic function as indicated by postexercise reductions of longitudinal strain, myocardial wall velocities, and FS were unrelated to a change in loading conditions (HR, and indirect measures of preload and postload) providing evidence of intrinsic decrements in myocardial performance. As such, the reductions in peak early
transmitral flow velocity and pulmonary vein atrial reverse flow duration are evidence of impaired LV relaxation.37 A novel finding in our work is the strong association of large artery compliance to altered ventricular function when adjusting for age and sex. It is well established that the interaction of the LV with the arterial system is a central determinant of cardiovascular performance and cardiac energetics.38 Furthermore, age-related decreases in LV systolic performance during exercise are associated with suboptimal ventricular–vascular coupling, the extent of which may differ between men and women.39 Thus, enhanced resting arterial compliance would support LV function during
TABLE 4. Tissue Velocities and LV Strain After PSE Pre-exercise Variable Tissue velocities E0 septal, m/s E/E0 septal† E0 lateral, m/s E/E0 lateral† E0 RV, m/s Strain/strain rate Longitudinal S, % Longitudinal SRsys, s21 Longitudinal SRdia, s21 Circumferential S, % Circumferential SRsys, s21 Circumferential SRdia, s21 Radial S, % Radial SRsys, s21 Radial SRdia, s21
Men
Postexercise Women
Men
Women
0.13 5.10 0.17 3.91 0.15
6 6 6 6 6
0.03 3.25 0.03 2.10 0.03
0.12 7.24 0.16 5.63 0.15
6 6 6 6 6
0.03 1.81 0.04 1.98 0.03
0.11 5.96 0.15 4.64 0.15
6 6 6 6 6
0.02* 1.03 0.04* 0.89 0.03
0.11 8.24 0.15 5.67 0.14
6 6 6 6 6
0.02* 2.02 0.04* 1.27 0.03
221.02 21.05 1.37 217.64 21.06 1.16 21.87 1.77 22.04
6 6 6 6 6 6 6 6 6
1.98 0.13 0.24 5.02 0.31 0.49 1.15 0.44 0.50
220.28 21.00 1.47 218.39 21.04 1.32 24.06 1.61 21.88
6 6 6 6 6 6 6 6 6
1.90 0.11 0.24 5.24 0.32 0.58 4.02 0.46 0.72
218.44 21.08 1.29 217.69 21.25 1.15 24.57 1.94 22.06
6 6 6 6 6 6 6 6 6
0.34* 0.18 0.30 4.95 0.33 0.43 4.95 0.46 0.67
218.44 21.02 1.52 218.49 21.10 1.44 22.10 1.84 22.38
6 6 6 6 6 6 6 6 6
2.34* 0.22 0.31 4.59 0.25 0.56 1.52 0.51 0.50
*From pre-exercise. †P , 0.05 between men and women. E0 , myocardial tissue velocity; E, peak early transmitral flow velocity; RV, right ventricle; S, strain; sys, systolic; dia, diastolic.
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Clin J Sport Med Volume 25, Number 3, May 2015
FIGURE 2. Association between resting arterial compliance and percent change in LV septal wall tissue velocities (A), LV lateral wall tissue velocities (B), and longitudinal strain (C) after PSE. Dark circles indicate men; open circles, women.
strenuous exercise, as is indicated by lower relative decrements in LV strain and tissue velocities postexercise. Improved arterial compliance and subsequent LV performance may be linked to training status. Endurance training increases arterial compliance and has also been shown to attenuate age-related declines in large artery compliance.40 Further evidence of training status in our cohort may be inferred from measures of race pace and lifetime ultramarathons to represent aspects of aerobic capacity and chronic training, respectively. Cardiac output and perfusion pressure are compromised in untrained individuals when both the metabolic and thermoregulatory demands are high.41 In a meta-analysis reviewing LV function with ultraendurance exercise, one of the factors influencing a decline in systolic function was poor training status.7 Thus, our findings suggest that greater training experience, and subsequent improvements in fitness, may Copyright © 2014 Wolters Kluwer Health, Inc. All rights reserved.
Cardiac Sex Differences and PSE
reduce the cardiovascular strain that may accompany ultraendurance exercise. However, recent reports of myocardial fibrosis in veteran endurance athletes,15,42,43 linked to years of training competing,15 do not support our speculation. The efficacy and potential risks of long-term endurance training remain in question.10 Interestingly, although not all investigations have found evidence of exercise-induced cardiac fatigue after PSE, there have been reports of reduced radial, circumferential and longitudinal strain, and SRs in ultra-events.28,36 In the present investigation, reductions in LV tissue velocities and longitudinal strain did not extend to the radial and circumferential planes. Ventricular dysfunction has been suggested to begin in the longitudinal plane while circumferential and radial compensations remain to preserve EF under stress.44 Thus, in the present investigation, cardiac fatigue may be described as moderate in comparison with events of similar magnitude.28,36 Because exercise duration may be associated with exercise-induced cardiac fatigue,5,6,45 it was expected that this ultramarathon occurring in an extreme mountain terrain environment would have induced greater impairments in ventricular function. Temperature and intensity may be contributing factors. In the Western States Endurance Race,28 racers presumably had much higher thermal strain to contend with than our temperate mountain race. Heat stress translocates blood volume from the centre to the periphery, for which the demand for skin blood flow is met in part by an increase in CO.46 However, over the course of the ultramarathon, competing demands for blood flow between working musculature and skin perfusion and may alter the myocardial perfusion-towork relationship, leading to impaired myocardial function.41 Alternatively, the extreme mountainous terrain of the Fat Dog 100 may have induced considerable neuromuscular fatigue47 and as a result lowered exercise intensity enough to spare cardiovascular fatigue. Mattsson et al48 recently showed that when exercise duration exceeds 24 hours, cardiac work (stroke work · HR) and myocardial oxygen consumption decrease, likely as a physiological adaptation to maintain CO when total energy expenditure demands are high. The relative contribution of these factors on LV function with PSE requires further research. A limitation of this investigation is the small sample of female subjects relative to the males. Recruitment of participants in field studies is limited to those runners who wish to participate. Because ultraendurance competitors are typically only 20% female,16 it becomes increasingly difficult to study females in numbers relative to males. After attrition, females represented 32% of our cohort, which is in proportion to the female racers participating in the event. Posteriori calculations revealed a moderate effect size consistent across most variables (h = 0.28-0.67). Interestingly, we have previously reported sex differences following laboratory-based investigations of strenuous exercise using similar sample sizes,17,33 thus, we do not believe this factor impacted our results, although we cannot exclude the possibility of a type II error. In concert with the same recruitment issues, it is also not possible to recruit based on fitness. Our sample included the first place finisher completing the race in 28 hours with our last finisher coming in at 41 hours. Because logistical issues limited the assessment of www.cjsportmed.com |
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each participant’s aerobic capacity, we are unable to determine whether the men and women were equal with respect to relative V̇ O2max. Nonetheless, we are confident in our use of race pace and race time as surrogate measures of fitness status, and such practice has been reported by others.49 Another consideration is the prevalence of sodium supplementation in our sample of ultramarathoners. In this study, we were unable to control for the form, quantity, and frequency of sodium ingested. Sodium loading has been shown to increase plasma volume at rest and reduce physiological strain in warm conditions, significantly improving exercise capacity.50 How sodium affects exercise-induced cardiac fatigue is not known and should be the focus of future investigations exploring exercise-induced cardiac fatigue. The results of this investigation suggest that in response to an acute bout of PSE, cardiac adjustments are similar in men and women. Independent of sex, we present indications for reduced cardiovascular strain associated with indices of enhanced vascular health and greater training experience. Considering recent clinical concerns pertaining to the effects of PSE on the heart, further research is required to delineate the impact of acute and chronic exposure to PSE on LV function and long-term cardiac health.
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ACKNOWLEDGMENTS The authors acknowledge Dr. Jack Taunton and GE Healthcare for their technical expertise in this project. REFERENCES
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