Left Ventricular Fibrosis in Middle-Age Athletes and Physically Active Adults : Medicine & Science in Sports & Exercise

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Left Ventricular Fibrosis in Middle-Age Athletes and Physically Active Adults


Author Information
Medicine & Science in Sports & Exercise: December 2020 - Volume 52 - Issue 12 - p 2500-2507
doi: 10.1249/MSS.0000000000002411


Exercise training is known to elicit morphological cardiac adaptations including chamber enlargement and modest hypertrophy, often termed the athlete’s heart (1). Apart from contributing to enhanced cardiorespiratory fitness, favorable cardiac remodeling is largely considered to be a desired outcome of endurance training (2). However, concerns persist that adverse cardiac remodeling may occur secondary to long-standing endurance exercise that is performed well-beyond recommended levels (3–5), including the promotion of a proarrhythmic phenotype and myocardial damage. Reports of focal left ventricular (LV) myocardial fibrosis in elite and subelite, recreational endurance athletes (EA) using cardiac magnetic resonance (CMR) late gadolinium enhancement (LGE) imaging are equivocal, with approximately 8% of studies reporting evidence of focal LV fibrosis (6–16), yet many have failed to detect any such evidence (17–24). More recently, a limited number of studies have assessed the presence of diffuse myocardial fibrosis (via native T1 and extracellular volume (ECV)) in primarily male athletes of varying age and variable training history (11,12,15,16,25,26). An early report showed no association between LV mass and an expanded ECV (15), whereas a recent report described a marginally higher ECV among EA with focal fibrosis (11).

Although some of these studies are limited by their small sample of EA with LGE (12,15,16,25) or limited phenotypic data describing exercise capacity and/or training history of participants (15), a key gap in this literature is reflected by the focus on younger athletes (11,12,25), providing only limited data on the long-standing middle-age subelite “recreational” athletes (11,14) who actually represent the largest and fastest growing cohort of endurance exercise participants (16,27). Moreover, existing studies have largely compared findings to sedentary cohorts (10,12,13,15–17) rather than physically active (PA), age-matched individuals who have performed vigorous exercise over a similar period of time, but only at recommended levels. Such an approach would help determine if adverse remodeling is the result of “excessive” exercise performed over many years by EA, or if it is epiphenomena to “typical” exercise that is widely advocated and linked to long-term positive cardiovascular outcomes (28), yet accrues a lower exercise burden over a similar period of time.

Therefore, we sought to perform detailed phenotypic profiling and CMR with LGE and T1 mapping to evaluate cardiac morphology including the presence of LV focal LGE and diffuse myocardial remodeling as assessed by ECV in healthy, middle-age, subelite recreational EA and age-matched PA adults who have performed regular exercise within guideline recommendations for a similar time period. We hypothesized that the prevalence of ventricular LGE would be higher in the EA group and be positively correlated to cardiac structural indices and cumulative training hours.


General study procedures

Middle-age adults between 45 and 65 yr old were recruited from the local community (see Figure, Supplemental Digital Content 1, Consort flow diagram for athlete’s heart study, https://links.lww.com/MSS/C12). All EA athletes were from local running, cycling, and triathlon clubs, recruited from notices posted in local marathon blogs and e-mail announcements to members sent by club organizers. All had at least 10 yr of regular competitive endurance participation (e.g., running, cycling, and/or triathlon) and maintained their club memberships with regular participation over a minimum of 10 yr. Runners performed weekly mileage greater than 40 km with participation in at least one annual marathon or event of a greater duration. Cyclists had weekly mileage in excess of 300 km with participation in annual races more than 100 km. Triathletes trained and competed in short-course, half or full Ironman competitions annually and may have competed in singular cycling and/or running events similar to that reported by cyclists or runners. The PA participants were recruited separately (from community and university fitness facilities), provided they had reported consistent, long-standing physical activity/participation in fitness classes or mixed physical activity modalities that may have included jogging or incidental cycling. All were required to approach or meet, but not exceed, current Canadian physical activity guidelines (150 min·wk−1 of moderate-to-vigorous physical activity (29). Participants who took part in regular organized fun runs or similar events exceeding 5 km were excluded. Additional exclusion criteria for all participants included resistance training >3 h·wk−1, any cardiac-related symptoms and/or disorder, diabetes, history of thyroid disorder, sleep apnea or any reported sleep disordered breathing, chronic inflammatory disease, smoking history within the past 10 yr, recreational drug use, or excessive alcohol consumption. The study was approved by institutional research ethics boards, conforming to the Declaration of Helsinki on the use of human participants with written informed consent obtained from participants before study participation.

Initial assessments included a full medical and exercise training history, in addition to a 2-wk exercise diary, which included detailed written descriptions of exercise mode, and duration and intensity for each work workout. To confirm the presence (or absence) of a consistent 10-yr training period described in their training histories and 2-wk diary, a Likert scale was used (1–2, “significantly less exercise than before”; 3–4, “slightly less exercise than before”; 5–6, “about the same amount of exercise”; 7–8, “slightly more than before”; 9–10, “significantly more than before”). Basic anthropometric measures and graded exercise testing were also assessed. Participants were classified as EA or PA by self-identification, verified by their exercise diaries.

Peak oxygen consumption

Before graded exercise testing, resting blood pressure (BP) was obtained using standard procedures (BpTRU model BPM-100; BpTRU Medical Devices, Coquitlam, BC, Canada). Peak oxygen uptake (peak V̇O2) was then determined as the highest 20-s average of oxygen consumption obtained using a treadmill and metabolic cart (Moxus Modular V̇O2 system; Applied Electrochemistry Inc., Pittsburgh, PA) and a 12-lead electrocardiogram (Philips StressVue Stress Testing System; Philips Medical System, Andover, MA). Two-minute stages were performed with a self-selected constant speed and increases in treadmill grade (in percent) until exhaustion.


A standardized CMR examination was performed using a 3.0-T magnetic resonance imaging scanner (Siemens MAGNETOM Skyra 3.0 T with TIM and DOT technology) with a phased-array cardiac coil and retrospective electrocardiographic gating, and images obtained on end-expiration breath-holds. A short-axis stack and long-axis views (two- and four-chamber) were acquired to analyze LV and right ventricular (RV) mass, dimensions, and function. LGE was assessed after the gadolinium injection (0.1 mmol·kg−1 body weight, Multihance (Bracco Diagnostic Inc., Princeton, NJ) or gadolinium-diethylene triamine pentaacetic acid, 0.2 mmol·kg−1 (Gadovist, Bayer Healthcare, Wayne, NJ). Athletes (n = 18) who received Multihance demonstrated abnormalities during initial evaluation, which required further clarification (i.e., abnormal ECG or echocardiogram) and were therefore scanned under a clinical protocol. The remainder (n = 74) were scanned under the research protocol and received Gadovist. All scans were performed on the same Siemens 3 T Skyra. Furthermore, the timing of Multihance injection was exactly the same as for the Gadovist, as the protocol and sequences were identical. Short-axis and long-axis images (two- and four-chamber) were acquired ensuring whole heart coverage to determine the presence of LGE using a TrueFISP IR single-shot and phase-sensitive inversion recovery sequence.

T1 mapping was performed in a single LV midventricular slice, excluding LGE lesions and subepicardial and subendocardial pixels, using a Modified Look-Locker Inversion recovery sequence before and after the gadolinium contrast administration (echo time of 1.1 ms, spatial resolution of 1.4 × 1.4 mm, and slice thickness of 8 mm, voxel size of 1.4 × 1.4 × 8 mm, field of view of 360 mm, flip angle was 35°, repetition of 308.76 ms) (30). A motion-correction algorithm was applied to compensate for any patient movement. Hematocrit (Hct) was measured before scheduled echocardiographic assessment, on a separate day from the CMR examination. All subjects undertook Hct in the seated position, and on the day of examination (both echocardiogram and CMR), athletes were advised to not perform exercise. In between blood draw and CMR, all athletes remained clinically stable. Normal values for CMR end points in adults, including ECV and T1, have been reported previously (31–35).

All CMR volumetric end points were measured by a single reader blinded to other clinical data using commercially available software, with particular care to exclude papillary muscles and artifact (CVi42 Version 5.1; Circle Imaging, Calgary, Canada). Ventricular mass and function were determined with a manual tracing of the endocardial and epicardial borders. LGE was evaluated by two expert CMR readers blinded to clinical data, and consensus was reached. RV hinge-point LGE was evaluated by cross-referencing the short-axis image with long-axis imaging planes to ensure LGE signal was within the myocardium and not partial voluming from the blood pool. Global and segmental T1 mapping included a manual tracing of the endocardial and epicardial borders and blood pool with image quality assessed. Manual regions of interest were placed in the interventricular septum, as well as inferior RV hinge point in order to assess regional interventricular T1 values before and after contrast, which were Hct corrected and used to determine regional ECV. The region of interest was optimized to be a consistent size and location. All contours and manual region of interest were reviewed by K.C. for consistency, as reported by Dabir et al. (36). Image quality was scored as reported by Kellman et al. (37), with three participants removed from analysis because of inadequate image quality. Overall, after three participants were removed, 88% received a score of 5 and 12% a score of 4 (out of 5).

Statistical analysis

Descriptive statistics were reported as mean ± SD for normally distributed data or as median (interquartile range) for nonnormally distributed data. Independent-sample t-tests were used to assess the statistical significance between study groups (EA and PA) and sex (male vs female). χ2 Tests were also performed to examine the association between the presence and type of LGE, and study groups and sex. Pearson r correlation analysis was performed to examine the factors associated with cardiorespiratory fitness (peak V̇O2) and T1 mapping indices (T1 native, T1 postcontrast administration, and ECV). Interobserver variability was calculated and presented as correlation and Bland–Altman plots (Figure, Supplemental Digital Content 2, T1 native data, https://links.lww.com/MSS/C13). Statistical significance was determined a priori (P < 0.05), and Bonferroni correction was used to control for multiple comparisons. Analyses were performed using statistical software (version 9.4; SAS Institute, Cary, NC).


Participant demographics

A total of 92 participants completed the study (Table 1; n = 72 EA and n = 20 PA). EA participants were identified as runners (n = 24), cyclists (n = 20), and triathletes (n = 28).

TABLE 1 - Participant demographics by group.
EA PA Adults
All (n = 72) Male (n = 53) Female (n = 19) All (n = 20) Male (n = 9) Female (n = 11)
Age, yr 53 ± 5* (*P = 0.01) 54 ± 5 52 ± 5** (**P = 0.02) 56 ± 4 57 ± 4 56 ± 4
Resting systolic BP, mm Hg 114 ± 15 118 ± 14*** (***P = 0.0003) 103 ± 10 113 ± 15 114 ± 12 112 ± 17
Resting diastolic BP, mm Hg 74 ± 10 76 ± 9*** (***P = 0.002) 68 ± 10 72 ± 8 72 ± 8 73 ± 9
Resting heart rate, bpm 53 ± 10 50 ± 10 59 ± 8 65 ± 8 59 ± 8 68 ± 6
BSA, m2 1.9 ± 0.2 1.9 ± 0.1*** (***P < 0.0001) 1.6 ± 0.2 1.9 ± 0.2 2.0 ± 0.1*** (***P = 0.0002) 1.7 ± 0.2
Whole body mass, kg 72 ± 13 76 ± 10*** (***P = 0.0001) 59 ± 10 73 ± 15 85 ± 10*** (***P < 0.0001) 64 ± 11
Hct, % 42 ± 3 43 ± 3 39 ± 3 41 ± 3 43 ± 3 39 ± 1
Maximal exercise capacity (V̇O2max), mL·kg−1·min−1 50 ± 7* (*P < 0.0001) 51 ± 7** (**P < 0.001) 49 ± 7** (**P < 0.0001) 37 ± 9 40 ± 9 35 ± 9
Systolic BP during maximal exercise, mm Hg 199 ± 28 203 ± 24 189 ± 33 205 ± 22 207 ± 20 194 ± 25
Diastolic BP during maximal exercise, mm Hg 93 ± 15 95 ± 13 88 ± 14 96 ± 24 100 ± 24 91 ± 24
Weekly hours of vigorous exercise, h 7.6 ± 4.5* (*P < 0.0001) 7.8 ± 4.8** (**P < 0.0001) 6.2 ± 2.9** (**P = 0.02) 2.4 ± 3.1 1.7 ± 1.9 2.1 ± 2.8
Data have been presented as mean and SD.
*P < 0.05 for between-group comparisons of EA and PA.
**P < 0.05 for within-sex comparisons of EA and PA.
***P < 0.05 for within-group comparisons of male and female participants.

Cardiac structure and function

Structural parameters and ejection fractions (EF) are categorized by group and sex (Table 2). Briefly, the EA group had a higher peak V̇O2, a trend toward greater LV and RV volumes, and cardiac mass when compared with PA, but no between-group differences were observed in LV EF and RV EF. Among EA versus PA male participants, there were no differences in LV and RV indices and mass index, with the exception of LV end-diastolic volume index. A greater LV and RV mass index was observed in EA versus PA female participants. Among all participants, a higher peak V̇O2 was positively associated with younger age (r = −0.30, P = 0.005), greater weekly hours of vigorous exercise (r = 0.29, P = 0.008), and indexed cardiac structural measures of LV end-diastolic volume (r = 0.59) and end-systolic volume (r = 0.55), LV mass (r = 0.54), and RV mass (r = 0.49;P < 0.0001 for all).

TABLE 2 - CMR-derived cardiac structure and function by physical exercise history.
EA PA Adults
Variable All
(n = 72)
(n = 54)
(n = 19)
(n = 20)
(n = 9)
(n = 11)
Left ventricle
 End-diastolic volume indexed to BSA, mL·m−2 103 ± 15* (*P = 0.0005) 105 ± 15**,*** (**P = 0.003, ***P = 0.02) 94 ± 13*** (***P = 0.005) 85 ± 14 93 ± 9** (**P = 0.009) 78 ± 14
 End-systolic volume indexed to BSA, mL·m−2 45 ± 8* (*P = 0.0002) 46 ± 8** (**P = 0.005) 40 ± 6*** (***P = 0.01) 36 ± 7 40 ± 5** (**P = 0.03) 33 ± 8
 LV mass indexed to BSA, g·m−2 63 ± 11* (*P < 0.0001) 67 ± 9** (**P < 0.0001) 52 ± 11*** (***P = 0.003) 50 ± 13 61 ± 9** (**P < 0.0001) 41 ± 7
 EF, % 57 ± 4 57 ± 4 58 ± 3 58 ± 4 57 ± 3 58 ± 4
Right ventricle
 End-diastolic volume indexed to BSA, mL·m−2 112 ± 18* (*P = 0.001) 116 ± 18** (**P = 0.001) 99 ± 14 92 ± 14 102 ± 11** (**P = 0.002) 84 ± 11
 End-systolic volume indexed to BSA, mL·m−2 54 ± 13* (*P = 0.004) 56 ± 13** (**P < 0.0001) 45 ± 8 43 ± 8.4 49 ± 7** (**P = 0.001) 38 ± 6
 RV mass indexed to BSA, g·m−2 19.0 ± 3.5* (*P = 0.0004) 20 ± 3** (**P = 0.007) 17 ± 4*** (***P = 0.002) 15.7 ± 3.4 19 ± 2.2** (**P = 0.0001) 13 ± 1.8
 EF, % 53 ± 4 52 ± 5** (**P = 0.001) 55 ± 3 54 ± 4 52 ± 3 55 ± 5
Data have been presented as mean and SD.
*P < 0.05 for between-group comparisons of EA and PA.
**P < 0.05 for within-group comparisons of male and female participants.
***P < 0.05 for within-sex comparisons of EA and PA.

Presence of LGE

The CMR LGE protocols were performed in a subset of participants (LGE, n = 89; T1 mapping, n = 66) because of participant noncompliance (e.g., refusal of gadolinium administration) and technical issues (e.g., magnetic resonance imaging scheduling; poor image quality, n = 3). Focal LV LGE was observed in 30% of (n = 27/89) participants, including EA (n = 23/69; 33%) and PA (n = 4/20; 20%) participants. LGE was observed either at the RV hinge point (n = 21/89; 23.5%) or classified as ischemic (n = 2/89; 2%) and nonischemic origin (n = 4/89; 4%). LGE of ischemic and nonischemic origin were found in EA male participants only. The proportion of EA with LGE did not differ by sex (male vs female: n = 18/53 (34%) vs n = 5/16 (31%), P = 0.84), group (EA n = 23/69 (33%) vs PA = 4/20 (20%), P = 0.25), or type of EA (runner: n = 24 (33%) vs cyclist: n = 20 (39%) vs triathlete: n = 28 (32%) vs PA: n = 20 (20%), P = 0.45). Among all participants with and without LGE, no between-group differences in demographics (age, BP, peak V̇O2, weekly hours of vigorous exercise), and ventricular volume, ventricular mass indices, and EF were found (Fig. 1).

Representative images of cardiac LGE in middle-age athletes. A, RV hinge-point LGE. B, Nonischemic LGE. C, Ischemic LGE. D, Native T1 mapping.

T1 mapping data are summarized in Table 3. Briefly, there was no difference in global precontrast, postcontrast T1 values, or ECV values between EA and PA. When a regional analysis was performed, EA tended to have higher, albeit within normal range, regional ECV at the interventricular septum and RV hinge point (Table 3). Regional precontrast values in the interventricular septum and RV hinge point were not different between groups. Postcontrast T1 values were numerically lower in the PA group but not statistically different. The heterogeneity of the global ECV values is shown by group in Figure 2. A higher global ECV was not associated with LV mass indexed to body surface area (BSA) (r = 0.02, P = 0.87). No differences in T1 mapping data (T1 native or global ECV) were observed among participants with and without LGE. Notably, participants with and without T1 mapping did not differ in demographics or cardiac structural parameters.

TABLE 3 - CMR assessment of diffuse cardiac fibrosis by group.
Variable EA PA
All (n = 50) Male (n = 38) Female (n = 12) All (n = 16) Male (n = 9) Female (n = 7)
T1 native data
 Global myocardial, ms 1169 ± 35 1164 ± 36 1190 ± 23 1190 ± 26 1183 ± 26 1197 ± 22
 Interventricular septum T1, ms 1178 ± 34 1173 ± 37 1193 ± 16 1195 ± 31 1186 ± 37 1205 ± 21
 RV hinge-point T1, ms 1201 ± 46 1192 ± 49* (*P = 0.001) 1228 ± 23 1214 ± 52 1192 ± 53 1240 ± 41
T1 postcontrast administration
 Global myocardial, ms 366 ± 44 375 ± 79** (**P = 0.01) 339 ± 31 334 ± 36 324 ± 35 340 ± 38
 Interventricular septum T1, ms 355 ± 50 363 ± 50 330 ± 42 332 ± 43 325 ± 43 340 ± 44
 RV hinge-point T1, ms 353 ± 49 360 ± 53 333 ± 29 319 ± 43 317 ± 54 322 ± 31
ECV fraction data
 Global ECV, % 22.6 ± 3.5 22.1 ± 3.3 24.2 ± 3.9 21.5 ± 2.6 22.3 ± 3.3 20.4 ± 2.8
 Interventricular septum ECV, % 22 ± 8*** (***P = 0.002) 22 ± 9** (**P = 0.003) 25 ± 8** (**P = 0.005) 16 ± 3 17 ± 3 16 ± 4
 RV hinge-point ECV, % 23 ± 7 22 ± 7 25 ± 7** (**P = 0.007) 18 ± 4 18 ± 4 17 ± 3
Data presented as mean ± SD. Significance indicated for the following comparisons.
*P < 0.05 for sex-based within-group comparisons.
**P < 0.05 for within-sex comparisons of EA and PA.
***P < 0.05 for between-group comparisons of EA and PA.

Scatterplot of global ECV (in percent) by group.


In a cohort of middle-age EA compared with PA, we have demonstrated normal physiologic morphological LV adaptions consistent with the “athlete’s heart.” Although nearly one-third of both EA and PA participants demonstrate LGE, this was primarily confined to the RV hinge point. Further detailed myocardial tissue characterization using T1-mapping analysis revealed no evidence of diffuse remodeling as assessed by ECV or significant relationship between LV mass and expanded ECV among our healthy athletic cohort. Our study offers novel observations not previously reported, including data from a cohort of subelite, middle-age EA participants with a long-standing history of intensive endurance sport practice (>3-fold current weekly physical activity recommendations), with comparison to a PA control group matched for years of regular physical activity, but performed only at recommended levels that have been associated with favorable cardiovascular outcomes. Despite significant heterogeneity in exercise training history, we have demonstrated that LGE was observed with similar frequency in both EA and PA, which suggests that LGE may be epiphenomenon to a broad exercise burden, given the favorable long-term cardiovascular outcomes recently observed in those exercising at or well-beyond recommended levels of exercise.

The observed LGE findings were primarily confined to the RV inferior hinge point, consistent with previous reports (8,38), with a similar degree of focal RV hinge-point LGE between male and female EA, despite negligible differences in cardiorespiratory fitness, exercise training volume, or exercise modality. These observations were also unrelated to resting or exercise BP, cardiac volumes, and mass, or T1 mapping data. The mechanisms promoting exercise-related RV hinge-point LGE remain poorly understood. It has been hypothesized that genetic predisposition (39) and silent myocarditis (40) may cause hinge-point fibrosis; however, it has also been identified in otherwise healthy adults. It is unknown if exercise per se can trigger this response. Sustained elevations in RV afterload during exercise stress have been shown to be associated with fibrosis at sites of RV septal attachment (39), and earlier reports have suggested that endurance exercise elicits excessive elevations in pulmonary pressures in response to intensive exercise (41). However, more recent data from our group demonstrated that, although acute exercise significantly elevates pulsatile RV afterload, pulmonary vascular resistance falls with only modest increases in pulmonary arterial pressures (42,43), which are not exacerbated with sustained during prolonged exercise (44). Although the current study demonstrates increases in RV mass and volumes in EA, this is likely a physiologic adaption, influenced by the nature of exercise and related hemodynamic overload sustained by the RV (45). Unfortunately, the spatial resolution of our LGE sequence prevented the accurate identification of RV LGE, or change in RV ECV, nor did we calculate pulmonary vascular resistance. Further research focusing on detailed RV tissue characterization is required to determine if the hinge point is under greater mechanical stress and is a vulnerable location for fibrotic development in both exercise and disease, and what effect repeated elevations in RV afterload as a result of intensive exercise may have on the remodeling process.

Overall, we observed a higher proportion of LGE in long-standing EA compared with the majority of prior studies of EA (6–15), whereas Tahir et al. (11) report higher LGE prevalence in younger male triathletes. A small number of our EA exhibited focal LV LGE reflecting a pattern typical of fibrosis secondary to ischemic and nonischemic injury (n = 6/86), but it remains unknown if these findings were consistent with previous impairments in coronary blood flow and/or myocardial infarction or myocarditis, or simply reflected an unusual pattern of remodeling in response to exercise-induced hemodynamic loading (46). Our studies differ from prior studies in that these data were from a limited sample of athletes with LGE and included female EA with significantly lower cardiorespiratory fitness and training volumes (11). Therefore, it is likely that relatively small sample sizes and disparate populations in these studies account for these differences.

Recent evidence also indicates that LGE may be more common in athletes with exercise-induced hypertension (11), and these observations have recently led to speculation that “exercise ‘hypertension” and or exaggerated BP responses to exercise, along with exercise-induced volume overload, in athletes may lead to LV fibrosis, along with chronic exercise-induced volume overload (47). Exaggerated BP elevation with exercise may not be uncommon in athletes (48). In the present study, LGE in either EA or PA was independent of resting or exercise (maximal exercise test) BP response, and previous work by our group has demonstrated that athletes with exaggerated BP have well-matched ventricular-vascular coupling during exercise (49).

Mild reductions in global radial, but not longitudinal LV resting strain, have been weakly associated with LGE extent among triathletes with normal resting LV EF (50). However, disparate regional myocardial contractile profiles and a lack of differences in these measures between athletes and control groups make interpretation of these findings difficult. Therefore, in the absence of clinically relevant reductions in cardiac function, symptoms, or impairment of exercise performance, the present findings further support the concept that hinge-point LGE may represent benign, physiologic remodeling in response to chronic exposure a wide range of exercise, from exercise performed at or well-beyond recommended levels. Establishing a dose–response of the exercise burden and the presentation of LGE, and whether this is benign or elicits long-term pathological responses, requires long-term follow-up studies.

T1 mapping studies in athletes have primarily examined younger individuals (11,12,15,25). One recent study failed to observe differences in ECV in middle-age male runners relative to sedentary adults (16). In the present study, we report normal values for T1 mapping and global ECV fractions; in fact, EA tended to have lower T1 native values relative to PA, suggesting that the higher cardiac mass among EA was secondary to myocyte hypertrophy rather than ECV expansion; this was particularly evident among our larger sample of male participants. In addition, our female EA tended to have marginally higher T1 native values (nonsignificant) but similar ECV when compared with male EA. Higher T1 native and ECV values in older, untrained female participants have been reported previously and may be due to their smaller cardiac structure and potential for partial volume effects of the blood pool (51). Studies examining the acute effects of prolonged exercise have failed to demonstrate postrace differences of T2 and T1 relaxation times in runners (24) and, most recently, triathletes (52). However, differences in training state, timing of CMR scanning, and postexercise hydration states make comparisons between studies challenging. The latter study (age range, 18–61 yr) suggested that a reduction in left atrial EF in LGE-positive triathletes may relate to higher BP responses to exercise testing, yet our data found no such relationship. Our present data suggest that long-standing endurance training is characterized by physiological, not pathological myocyte remodeling (1,38,53). We were unable to detect sex differences in ECV between male or female EA, and larger studies powered to assess sex differences are required.


The smaller PA sample size may have been underpowered, especially for sex-based analyses. Quantifying long-term training history is challenging, as retrospective physical activity histories may be subject to recall bias; however, rather than reporting a simple measure of total hours of exercise over that time frame, we attempted to add precision by verifying the 10-yr training history against an immediate 2-wk training recall. Although we do not have a sedentary control group, we still identified significant adaptations in cardiac structure between EA and PA participants, consistent with “athlete’s heart” morphology (1). Our primary objective was to study the effect of exercise in EA relative to guideline-recommended levels. Whether LGE at either RV hinge point or the LV myocardium exists in an otherwise “healthy” cohort who do not exercise was not determined by this study, and therefore, further studies are required to determine the true incidence of such abnormalities in this population. We used two different contrast agents in the current study: Multihance and Gadovist. Although different contrast agents may affect the T1, the ratio of T1 precontrast and postcontrast is less susceptible to variation when expressed as ECV; hence, this is unlikely to account for the lack of change in global ECV seen between the EA and PA groups. Furthermore, although timing postcontrast administration is known to affect ECV, all persons underwent T1 mapping postcontrast within 20 min, which is unlikely to affect ECV (1). Hct estimation was performed on a separate day from the scheduled CMR examination. Timing of Hct is important in determining precise ECV measurements (54). Although this could result in greater variability in ECV estimation, all athletes ceased exercise on the day of examination and were clinically stable; hence, variability was minimized as much as possible (54). Finally, although there are numerical differences in the postcontrast T1 values in EA versus PA groups (Table 3), all values were within the normal range and not statistically different. These values fall within normal ranges based on our own data (unpublished) and published values (34,35). Whether these numerical differences are of clinical significance is beyond the scope of this study and requires assessment in a larger cohort with longer follow-up.


Focal LV LGE was observed in both EA (33%) and PA (20%) participants, located primarily at the RV hinge point. T1 mapping studies demonstrated no evidence of ECV expansion in the presence of normal cardiac remodeling. These data suggest that discrete ventricular LGE may be evident across a wide spectrum of cumulative exercise burden, independent of cardiac size or sex. In our cohort of EA performing higher-volume chronic endurance exercise, the finding of RV hinge-point LGE occurs in the absence of diffuse ECV expansion. Therefore, focal LV LGE may represent a benign process in otherwise healthy middle-age athletes. However, long-term follow-up studies are required to clarify the mechanisms contributing to RV hinge-point LGE in highly active middle-age adults and definitively exclude an association with pathology or increased risk for clinical events.

This study was funded by the Canadian Institutes of Health Research (fund no. 130477). Dr Laura Banks was supported by a Canadian Institutes of Health Research fellowship.

No conflicts of interest were declared. The results of the present study do not constitute endorsement by the American College of Sports Medicine. The results of the study are presented clearly, honestly, and without fabrication, falsification, or inappropriate data manipulation.


1. Pelliccia A, Caselli S, Sharma S, et al. European Association of Preventive Cardiology (EAPC) and European Association of Cardiovascular Imaging (EACVI) joint position statement: recommendations for the indication and interpretation of cardiovascular imaging in the evaluation of the athlete’s heart. Eur Heart J. 2018;39(21):1949–69.
2. Arbab-Zadeh A, Perhonen M, Howden E, et al. Cardiac remodeling in response to 1 year of intensive endurance training. Circulation. 2014;130(24):2152–61.
3. La Gerche A, Heidbuchel H. Can intensive exercise harm the heart? You can get too much of a good thing. Circulation. 2014;130(12):992–1002.
4. La Gerche A, Rakhit DJ, Claessen G. Exercise and the right ventricle: a potential Achilles’ heel. Cardiovasc Res. 2017;113(12):1499–508.
5. Elliott AD, La Gerche A. The right ventricle following prolonged endurance exercise: are we overlooking the more important side of the heart? A meta-analysis. Br J Sports Med. 2015;49(11):724–9.
6. Erz G, Mangold S, Franzen E, et al. Correlation between ECG abnormalities and cardiac parameters in highly trained asymptomatic male endurance athletes: evaluation using cardiac magnetic resonance imaging. Int J Cardiovasc Imaging. 2013;29(2):325–34.
7. Karlstedt E, Chelvanathan A, Da Silva M, et al. The impact of repeated marathon running on cardiovascular function in the aging population. J Cardiovasc Magn Reson. 2012;14:58.
8. La Gerche A, Burns AT, Mooney DJ, et al. Exercise-induced right ventricular dysfunction and structural remodelling in endurance athletes. Eur Heart J. 2012;33(8):998–1006.
9. Mangold S, Kramer U, Franzen E, et al. Detection of cardiovascular disease in elite athletes using cardiac magnetic resonance imaging. Rofo. 2013;185(12):1167–74.
10. Wilson M, O’Hanlon R, Prasad S, et al. Diverse patterns of myocardial fibrosis in lifelong, veteran endurance athletes. J Appl Physiol. 2011;110(6):1622–6.
11. Tahir E, Starekova J, Muellerleile K, et al. Myocardial fibrosis in competitive triathletes detected by contrast-enhanced CMR correlates with exercise-induced hypertension and competition history. J Am Coll Cardiol Img. 2018;11(9):1260–70.
12. McDiarmid AK, Swoboda PP, Erhayiem B, et al. Athletic cardiac adaptation in males is a consequence of elevated myocyte mass. Circ Cardiovasc Imaging. 2016;9(4):e003579.
13. Bohm P, Schneider G, Linneweber L, et al. Right and left ventricular function and mass in male elite master athletes: a controlled contrast-enhanced cardiovascular magnetic resonance study. Circulation. 2016;133(20):1927–35.
14. Breuckmann F, Mohlenkamp S, Nassenstein K, et al. Myocardial late gadolinium enhancement: prevalence, pattern, and prognostic relevance in marathon runners. Radiology. 2009;251(1):50–7.
15. Mordi I, Carrick D, Bezerra H, Tzemos N. T1 and T2 mapping for early diagnosis of dilated non-ischaemic cardiomyopathy in middle-aged patients and differentiation from normal physiological adaptation. Eur Heart J Cardiovasc Imaging. 2016;17(7):797–803.
16. Pujadas S, Donate M, Li CH, et al. Myocardial remodelling and tissue characterisation by cardiovascular magnetic resonance (CMR) in endurance athletes. BMJ Open Sport Exerc Med. 2018;4(1):e000422.
17. Abdullah SM, Barkley KW, Bhella PS, et al. Lifelong physical activity regardless of dose is not associated with myocardial fibrosis. Circ Cardiovasc Imaging. 2016;9(11).
18. Heidbuchel H, Hoogsteen J, Fagard R, et al. High prevalence of right ventricular involvement in endurance athletes with ventricular arrhythmias. Role of an electrophysiologic study in risk stratification. Eur Heart J. 2003;24(16):1473–80.
19. O’Hanlon R, Wilson M, Wage R, et al. Troponin release following endurance exercise: is inflammation the cause? A cardiovascular magnetic resonance study. J Cardiovasc Magn Reson. 2010;12:38.
20. Trivax JE, Franklin BA, Goldstein JA, et al. Acute cardiac effects of marathon running. J Appl Physiol. 2010;108(5):1148–53.
21. Mousavi N, Czarnecki A, Kumar K, et al. Relation of biomarkers and cardiac magnetic resonance imaging after marathon running. Am J Cardiol. 2009;103(10):1467–72.
22. Hanssen H, Keithahn A, Hertel G, et al. Magnetic resonance imaging of myocardial injury and ventricular torsion after marathon running. Clin Sci. 2011;120(4):143–52.
23. Gaudreault V, Tizon-Marcos H, Poirier P, et al. Transient myocardial tissue and function changes during a marathon in less fit marathon runners. Can J Cardiol. 2013;29(10):1269–76.
24. Scharhag J, Urhausen A, Schneider G, et al. Reproducibility and clinical significance of exercise-induced increases in cardiac troponins and N-terminal pro brain natriuretic peptide in endurance athletes. Eur J Cardiovasc Prev Rehabil. 2006;13(3):388–97.
25. Gormeli CA, Gormeli G, Yagmur J, et al. Assessment of myocardial changes in athletes with native T1 mapping and cardiac functional evaluation using 3 T MRI. Int J Cardiovasc Imaging. 2016;32(6):975–81.
26. Qasem M, George K, Somauroo J, et al. Influence of different dynamic sporting disciplines on right ventricular structure and function in elite male athletes. Int J Cardiovasc Imaging. 2018;34(7):1067–74.
27. Running USA. State of the Sport—US Road Race Trends 2016 [Available from: http://www.runningusa.org/state-of-sport-us-trends-2015. Accessed March 12, 2018.
28. Swift DL, Lavie CJ, Johannsen NM, et al. Physical activity, cardiorespiratory fitness, and exercise training in primary and secondary coronary prevention. Circ J. 2013;77(2):281–92.
29. Tremblay MS, Warburton DE, Janssen I, et al. New Canadian physical activity guidelines. Appl Physiol Nutr Metab. 2011;36(1):36–46; 47-58.
30. Piechnik SK, Ferreira VM, Lewandowski AJ, et al. Normal variation of magnetic resonance T1 relaxation times in the human population at 1.5 T using ShMOLLI. J Cardiovasc Magn Reson. 2013;15:13.
31. Kawel-Boehm N, Maceira A, Valsangiacomo-Buechel ER, et al. Normal values for cardiovascular magnetic resonance in adults and children. J Cardiovasc Magn Reson. 2015;17:29.
32. Kawel N, Nacif M, Zavodni A, et al. T1 mapping of the myocardium: intra-individual assessment of post-contrast T1 time evolution and extracellular volume fraction at 3T for Gd-DTPA and Gd-BOPTA. J Cardiovasc Magn Reson. 2012;14:26.
33. Roy C, Slimani A, de Meester C, et al. Age and sex corrected normal reference values of T1, T2 T2* and ECV in healthy subjects at 3T CMR. J Cardiovasc Magn Reson. 2017;19(1):72.
34. Weingartner S, Messner NM, Budjan J, et al. Myocardial T1-mapping at 3T using saturation-recovery: reference values, precision and comparison with MOLLI. J Cardiovasc Magn Reson. 2016;18(1):84.
35. Gottbrecht M, Kramer CM, Salerno M. Native T1 and extracellular volume measurements by cardiac MRI in healthy adults: a meta-analysis. Radiology. 2019;290(2):317–26.
36. Dabir D, Child N, Kalra A, et al. Reference values for healthy human myocardium using a T1 mapping methodology: results from the International T1 Multicenter cardiovascular magnetic resonance study. J Cardiovasc Magn Reson. 2014;16:69.
37. Kellman P, Wilson JR, Xue H, Ugander M, Arai AE. Extracellular volume fraction mapping in the myocardium, part 1: evaluation of an automated method. J Cardiovasc Magn Reson. 2012;14:63.
38. van de Schoor FR, Aengevaeren VL, Hopman MT, et al. Myocardial fibrosis in athletes. Mayo Clin Proc. 2016;91(11):1617–31.
39. Nielsen EA, Okumura K, Sun M, et al. Regional septal hinge-point injury contributes to adverse biventricular interactions in pulmonary hypertension. Physiol Rep. 2017;5(14).
40. Pressler A, Schmid A, Freiberger V, et al. Myocarditis, myocardial fibrosis and eligibility for competitive sports. Int J Cardiol. 2011;152(1):131–2.
41. D’Andrea A, Naeije R, D’Alto M, et al. Range in pulmonary artery systolic pressure among highly trained athletes. Chest. 2011;139(4):788–94.
42. Wright SP, Esfandiari S, Gray T, et al. The pulmonary artery wedge pressure response to sustained exercise is time-variant in healthy adults. Heart. 2016;102(6):438–43.
43. Wright SP, Granton JT, Esfandiari S, Goodman JM, Mak S. The relationship of pulmonary vascular resistance and compliance to pulmonary artery wedge pressure during submaximal exercise in healthy older adults. J Physiol. 2016;594(12):3307–15.
44. Buchan TA, Wright SP, Esfandiari S, et al. Pulmonary hemodynamic and right ventricular responses to brief and prolonged exercise in middle-aged endurance athletes. Am J Physiol Heart Circ Physiol. 2019;316(2):H326–34.
45. D’Ascenzi F, Pisicchio C, Caselli S, et al. RV remodeling in Olympic athletes. J Am Coll Cardiol Img. 2017;10(4):385–93.
46. Zorzi A, Perazzolo Marra M, Rigato I, et al. Nonischemic left ventricular scar as a substrate of life-threatening ventricular arrhythmias and sudden cardiac death in competitive athletes. Circ Arrhythm Electrophysiol. 2016;9(7):e004229.
47. Halle M, Esefeld K, Schindler M, Schunkert H. Exercise hypertension: link to myocardial fibrosis in athletes? Eur J Prev Cardiol. 2020;27(1):89–93.
48. Kim YJ, Kim CH, Park KM. Excessive exercise habits of runners as new signs of hypertension and arrhythmia. Int J Cardiol. 2016;217:80–4.
49. Currie KD, Sasson Z, Goodman JM. Vascular–ventricular coupling during exercise is not affected by exaggerated blood pressures in endurance-trained athletes. J Appl Physiol. 2019;127(3):753–9.
50. Tahir E, Starekova J, Muellerleile K, et al. Impact of myocardial fibrosis on left ventricular function evaluated by feature-tracking myocardial strain cardiac magnetic resonance in competitive male triathletes with normal ejection fraction. Circ J. 2019;83(7):1553–62.
51. Rosmini S, Bulluck H, Captur G, et al. Myocardial native T1 and extracellular volume with healthy ageing and gender. Eur Heart J Cardiovasc Imaging. 2018;19(6):615–21.
52. Tahir E, Scherz B, Starekova J, et al. Acute impact of an endurance race on cardiac function and biomarkers of myocardial injury in triathletes with and without myocardial fibrosis. Eur J Prev Cardiol. 2020;27(1):94–104.
53. Goodman JM, Banks L, Connelly KA, et al. Excessive exercise in endurance athletes: is atrial fibrillation a possible consequence? Appl Physiol Nutr Metab. 2018;43(9):973–6.
54. Engblom H, Kanski M, Kopic S, et al. Importance of standardizing timing of hematocrit measurement when using cardiovascular magnetic resonance to calculate myocardial extracellular volume (ECV) based on pre- and post-contrast T1 mapping. J Cardiovasc Magn Reson. 2018;20(1):46.


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