Impact Factor 6.050 | CiteScore 7.8
More on impact ›

ORIGINAL RESEARCH article

Front. Cardiovasc. Med., 12 May 2022 | https://doi.org/10.3389/fcvm.2022.882077

Longitudinal Associations Between Cumulative Physical Activity and Change in Structure and Function of the Left Side of the Heart: The Tromsø Study 2007–2016

  • 1School of Sport Sciences, UiT The Arctic University of Norway, Tromsø, Norway
  • 2Centre for Research and Education, University Hospital of Northern Norway, Tromsø, Norway
  • 3Department of Community Medicine, UiT The Arctic University of Norway, Tromsø, Norway
  • 4Department of Cardiology, Akershus University Hospital, Lørenskog, Norway
  • 5Institute of Clinical Medicine, University of Oslo, Oslo, Norway
  • 6Department of Clinical Medicine, UiT The Arctic University of Norway, Tromsø, Norway

Background: Current knowledge about the relationship between physical activity (PA) and cardiac remodeling is mainly derived from cross-sectional studies of athletes, and there is a knowledge gap of this association in the general adult and elderly population. Therefore, we aimed to explore the longitudinal association between cumulative PA and change in cardiac structure and function in a general adult and elderly population.

Methods: This longitudinal study includes 594 participants from the sixth (Tromsø6, 2007–08) and seventh (Tromsø7, 2015–16) survey of the Tromsø Study. Cardiac structure and function were assessed by echocardiography at two time points, and PA was self-reported by questionnaire at both time points. PA volume was expressed as cumulative PA (Low, Moderate, and Hard) and the association with left atrial (LA) and left ventricular (LV) structure and function was assessed using ANCOVA.

Results: Overall, LA diameter index (LADi) increased significantly more in Hard compared to Moderate PA (+0.08 cm/m2, 95% CI 0.01–0.15, p = 0.020) from Tromsø6 to Tromsø7. When stratified by sex or age, higher levels of cumulative PA were associated with increased LADi in males and in participants <65 years only. Indexed LV mass (LVMi) increased significantly more in Moderate than in Low PA (+3.9 g/m2.7, 95% CI 0.23–7.57, p = 0.037). When stratified by sex or age, these changes in LVMi and indexed LV diameter (LVDi) were only significant in females. No significant associations were observed between cumulative PA and change in relative wall thickness, E/e' ratio, e' velocity, LV ejection fraction, and LADi/LVDi ratio.

Conclusion: Higher levels of cumulative PA were associated with increased LADi in males and participants <65 years, and with increased LVMi and LVDi in females. Despite cardiac chamber enlargement, the pump function of the heart did not change with higher levels of PA, and the atrioventricular ratio was unchanged. Our results indicate that cardiac chamber enlargement is a physiological response to PA.

Introduction

Changes in cardiac structure and function can occur as a result of physiological remodeling from exercise or pathological remodeling (1). Whereas, physiological remodeling is considered benign adaptations, pathological remodeling is associated with increased risk of cardiovascular diseases and mortality. Both left atrial (LA) enlargement and left ventricular (LV) hypertrophy are independent risk factors for cardiovascular morbidity and mortality (24) in the general population, and occurs in response to risk factors such as hypertension, diabetes mellitus, and obesity via mechanisms such as increased pressure and volume overload (5).

Exercise-induced cardiac remodeling is generally considered a benign physiological adaption of exercise, and is characterized by enlarged cardiac chambers and increased LV wall thickness (6). Paradoxically, exercise-induced cardiac remodeling may mimic pathological remodeling (7, 8), and elite endurance athletes may have cardiac chamber size that overlap the size seen in cardiac pathology (7, 9, 10). However, it is observed that LA function (11, 12) and LV diastolic function (13, 14) are preserved in dynamic sport-elite athletes with LA enlargement, as well as in athletes with LV enlargement (7, 15).

Current knowledge about the relationship between physical activity (PA) and cardiac remodeling is mainly derived from cross-sectional studies of athletes (16), and there is a knowledge gap of this association in the general adult and elderly population. Hence, as most studies investigating the relationship between exercise and cardiac remodeling are cross-sectional, more longitudinal studies are needed. Therefore, our main objective was to explore the longitudinal association between cumulative PA and change in cardiac structure and function in a general adult and elderly population.

Materials and Methods

Study Population

The Tromsø Study is a single-center population-based cohort study with seven repeated health surveys of the population of the Tromsø municipality, Norway (17). This study includes participants from the sixth (Tromsø6, 2007–08) and seventh (Tromsø7, 2015–16) survey of the Tromsø Study.

In total, 623 participants provided valid data on self-reported PA in combination with valid echocardiography data from Tromsø6 and Tromsø7. We excluded participants with valvular heart disease at baseline (n = 21). Furthermore, eight participants were excluded due to missing data on the covariate hypertension. Finally, our analytical sample consisted of 594 participants free from valvular heart disease, and with valid data on PA, echocardiography, and covariates at baseline (Figure 1). However, the number of participants differed slightly between the different analyses due to missing images and/or due to images with inappropriate quality.

FIGURE 1
www.frontiersin.org

Figure 1. Flowchart over inclusion of participants: The Tromsø Study 2007–2016.

Physical Activity

PA was assessed using the Saltin-Grimby Physical Activity Level Scale (18), where the participants rank their leisure-time PA on a four-level scale. In our study, we summed up the participants' ranked leisure-time PA in Tromsø6 and Tromsø7 and combined them in a total cumulative score (Figure 2). Furthermore, we divided the cumulative score into three cumulative PA categories: (1) Low (total score 2–3), (2) Moderate (total score 4), and (3) Hard PA (total score 5-8).

FIGURE 2
www.frontiersin.org

Figure 2. Overview of summation of PA from Tromsø6 and Tromsø7 into cumulative PA categories: The Tromsø Study 2007–2016. PA: physical activity.

Cardiac Structure and Function

Echocardiographic examinations in Tromsø6 and Tromsø7 were performed by two qualified sonographers, for Tromsø6 collected from October 2007 to December 2008, using an Acuson Sequoia C512 (Acuson, Mountain View, California, USA) ultrasound scanner and for Tromsø 7 collected from August 2015 to October 2016 using a GE Vivid E9 (GE Medical, Horten, Norway) ultrasound scanner. The echocardiographic assessments were performed with the use of standard imaging planes in the left lateral decubitus position according to the joint American and European guidelines (19). In Tromsø6, the echocardiographic measurements were performed online in one heart cycle but remeasured if deviating from eye-balled estimates. In Tromsø7, the echocardiographic measurements were performed off-line on 3–5 consecutive cardiac cycles by a physician experienced in echocardiography (co-author MS), and the average was used in the analysis.

Cardiac dimensions were measured by M-mode echocardiography in the parasternal short axis view at the aortic valve level, after alignment of left ventricle in long axis view, according to the leading edge-to-leading edge convention (19). LV internal dimensions were measured at the end of diastole and systole and indexed to body surface area (LVDi) as cm/m2 (20). LA anteroposterior diameter was measured at the end of the LV systole and indexed to body surface area (LADi) as cm/m2. LA volume was measured at the end of the LV systole and calculated using the Simpson's biplane method from the apical four- and two chamber views and indexed to body surface area as mL/m2. LADi/LVDi ratio was calculated. Relative wall thickness was calculated with the formula (2 x posterior wall thickness) / (LV internal end-diastolic diameter). LV myocardial mass was calculated according to the cube formula (19), and further indexed to height by raising height to the power of 2.7 (LVMi), and are presented as g/m2.7 (21). LV ejection fraction (LV EF) was calculated using the Teichholz formula (22).

All Doppler examinations were performed in apical four-chamber view according to current recommendations (23). Mitral valve Doppler measurements were performed with a 2 mm Doppler sample volume placed between the mitral leaflet tips. Tissue Doppler measurements were performed with a 5 mm Doppler sample volume located at the septal and lateral side of the mitral annulus. Measurement of peak flow velocity in early diastole (E-wave) was measured with pulsed Doppler. Mitral annular e' velocity was measured with pulsed-wave tissue Doppler in both lateral and septal basal regions and furthermore averaged. E/e'ratio was calculated. Valvular heart disease was defined by the following criteria: (a) aortic stenosis (aortic valve mean gradient ≥15 mmHg) by continuous Doppler (24), (b) presence of mitral or (c) aortic regurgitation detected by color Doppler imaging with mitral insufficiency graded according to regurgitant jet area >4 cm2 (25), and aortic regurgitation graded by vena contracta width by color M-mode divided by of LV outflow tract diameter (>30% graded as moderate or higher) (25), and/or (d) mitral stenosis (E-wave deceleration time >350 msec and mitral E-wave >1 m/s) by pulsed Doppler (26). However, mitral stenosis was not identified in any subjects in our analytical sample.

In Tromsø7, an intra- and inter-observer study was performed on the echocardiography data (27). Intra-class correlation coefficients on Doppler indices and linear measurements were 0.90–0.99 in the intra-observer study and 0.84–0.98 in the inter-observer study. In Tromsø6, intra- and inter-observer variability on Doppler indices was evaluated by Bland-Altman analysis (24). The results showed mean inter-observer differences (95% limits of agreement) in the mean aortic gradient of −0.06 mmHg (−3.06 to 3.18). Intra-observer analysis gave a mean difference of −0.04 mmHg (−1.86 to 1.78) and 0.30 mm Hg (−3.96 to 4.56), respectively, in the two observers.

Covariates

Details about collection of baseline data are described elsewhere, and all data were collected by specially trained research technicians (28). Baseline data from Tromsø6 include the following covariates extracted from self-reported questionnaires, physical examinations, and blood samples: Daily smoking (yes or previously/never), diabetes (yes/no), use of antihypertensives (currently or previously/never), myocardial infarction (previously/no), stroke (previously/no). Alcohol consumption was the product of two questions, one reporting number of units of alcohol and one reporting frequency of drinking.

Blood pressure was recorded three times with 1 min intervals after 2 min seated rest with an automatic device (Dinamap Pro care 300 Monitor, GE Healthcare, Oslo, Norway), the average from reading two and three was used in our analyses. Blood pressure was classified into hypertension groups (21): (a) Normotensive (systolic blood pressure <140 mmHg, diastolic blood pressure <90 mmHg, and no self-reported use of antihypertensives), (b) hypertensive, controlled (systolic blood pressure <140 mmHg, diastolic blood pressure <90 mmHg, and self-reported use of antihypertensives), (c) hypertensive, uncontrolled (systolic blood pressure ≥140 mmHg and/or diastolic blood pressure ≥90 mmHg, and self-reported use of antihypertensives), or d) hypertension, untreated (systolic blood pressure ≥140 mmHg and/or diastolic blood pressure ≥90 mmHg, and no self-reported use of antihypertensives). Height and weight were measured to the nearest decimal with participants wearing light clothing and no footwear. Body mass index was calculated as weight (kg) divided by height squared (m2).

Data on atrial fibrillation was derived from the diagnosis registry of the University Hospital of North Norway, the only hospital in the region, by linking the hospitals records of atrial fibrillation to the participants' unique Norwegian national 11-digit identification number (29). Blood samples were analyzed for low-density lipoprotein (LDL) cholesterol at the Department of Clinical Chemistry, University Hospital of North Norway.

Statistical Methods

Descriptive characteristics of the study population are presented as means with standard deviations (SD) or percentages with number of observations (n). The associations between cumulative PA and cardiac structure and function were evaluated by one-way analysis of covariance with Bonferroni adjusted post hoc comparisons. Data are presented as adjusted means with standard error (SE), and effects with 95% confidence intervals (CI) unless otherwise stated. Model 1 is unadjusted, model 2 is adjusted for age, sex, body mass index, and hypertension groups.

Sex*PA was a significant interaction term in the association between PA and change in LA diameter (p = 0.024), body mass index*PA was a significant interaction term between PA and change in E/e' ratio (p = 0.028), and hypertension (normotensive/hypertensive)*PA was a significant interaction term between PA and change in average e' (p = 0.040).

To test the robustness of the fully adjusted model 2, we performed sensitivity analyses excluding participants with known cardiac pathologies (atrial fibrillation, myocardial infarction, stroke, and LV EF <40%) stepwise. Moreover, we performed sensitivity analysis adjusted for additional covariates (smoking, alcohol consumption, diabetes, and LDL cholesterol) stepwise added to the model.

For sensitivity analyses of the PA assessments, we compared the mean PA score in Tromsø6 with the mean PA score in Tromsø7, stratified by level of cumulative PA (Supplementary Table S1), to assess whether there were differences in PA score between Tromsø6 and Tromsø7 within each level of cumulative PA. Moreover, the activity level within each level of cumulative PA was quantified with accelerometry-measured PA, assessed by a triaxial accelerometer (wGT3X-BT, ActiGraph LLC, Pensacola, FL, USA), in Tromsø7 (Supplementary Table S2).

All statistical analyses were performed using SPSS version 28 (SPSS Inc., IL, USA), with a two-sided alpha ≤ 0.05 considered statistically significant.

Results

In total, 266 males (61.1 ± 8.9 years) and 328 females (58.9 ± 9.9 years), ranging from 37 to 76 years, were included in our study. Descriptive baseline characteristics of the analytical sample, stratified by PA, is given in Table 1.

TABLE 1
www.frontiersin.org

Table 1. Descriptive baseline characteristics stratified by level of cumulative physical activity: The Tromsø Study 2007–2008.

Overall, there was a significant difference in increase in LADi (p = 0.018) and LVMi (p = 0.037) between groups of cumulative PA in multivariate adjusted analyses (Supplementary Table S3). No significant differences were observed between cumulative PA and change in the other echocardiography variables (LVDi, relative wall thickness, E/e' ratio, e' velocity, LV EF, and LA/LV ratio) (Supplementary Table S3).

Cumulative PA and Change in LADi From Tromsø6 to Tromsø7

Overall, from Tromsø6 to Tromsø7, LADi increased significantly more in Hard compared to Moderate PA, with a mean group difference in LADi enlargement of 0.08 cm/m2 (95% CI 0.01–0.15, p = 0.020) (Table 2). No significant differences in LADi change were observed between Hard and Low PA (p = 0.128) and Moderate and Low PA (p = 1.000).

TABLE 2
www.frontiersin.org

Table 2. Longitudinal associations between cumulative physical activity and change in left atrial diameter index: The Tromsø Study 2007–2016.

In sex-stratified adjusted analysis (Table 2), LADi in males increased significantly more in Hard (0.30 cm/m2, SE 0.03) than in Moderate (0.14 cm/m2, SE 0.03) and Low PA (0.18 cm/m2, SE 0.04), with a mean group difference of 0.12 cm/m2 (95% CI 0.00–0.24, p = 0.047) between Hard and Low, and a mean group difference of 0.16 cm/m2 (95% CI 0.06–0.26, p < 0.001) between Hard and Moderate PA. No statistical difference between Moderate and Low PA was observed (p = 1.000). In females, no differences were observed (p = 0.852).

In age-stratified adjusted analysis (Table 2), LADi in participants <65 years increased significantly more in Hard (0.21 cm/m2, SE 0.03) than in Moderate (0.11 cm/m2, SE 0.03) PA, with a mean group difference of 0.10 cm/m2 (95% CI 0.01–0.18, p = 0.025). No statistical difference between Hard and Low PA (p = 0.474), or between Moderate and Low PA (p = 1.000) was observed. No statistical differences in LADi between groups were observed for participants ≥65 years (p = 0.262).

Associations between cumulative PA and cross-sectional LADi in Tromsø7 are presented in Figure 3. Significant associations between cumulative PA and LADi were observed in males, in participants <65 years, and in the overall analysis. Moreover, similar trends in the association between cumulative PA and LADi were observed in unadjusted, baseline adjusted, and in fully adjusted analysis. Associations between cumulative PA and cross-sectional LA volume index in Tromsø7 are presented in Figure 4. Significant associations between cumulative PA and LA volume index were observed in females, in participants <65 years, and in the overall analysis. Moreover, similar trends in the association between cumulative PA and LA volume index were observed in unadjusted, baseline adjusted, and in fully adjusted analysis.

FIGURE 3
www.frontiersin.org

Figure 3. Associations between cumulative PA and cross-sectional LA diameter index (LADi) in Tromsø7. (A) is unadjusted, (B) is adjusted for baseline LADi in Tromsø6, (C) is adjusted for baseline LADi in addition to age, sex, body mass index, and hypertension groups. Differences between groups of cumulative PA are indicated with p-values. Error bars indicate 95% CI. PA, physical activity; LA, left atrial; CI, confidence interval.

FIGURE 4
www.frontiersin.org

Figure 4. Associations between cumulative PA and cross-sectional LA volume index (LAVi) in Tromsø7. (A) is unadjusted, (B) is adjusted for baseline LADi in Tromsø6, (C) is adjusted for baseline LADi in addition to age, sex, body mass index, and hypertension groups. Differences between groups of cumulative PA is indicated with p-values. Error bars indicate 95% CI. PA, physical activity; LA, left atrial; CI, confidence interval; LADi, LA diameter index.

Cumulative PA and Change in LVMi From Tromsø6 to Tromsø7

Overall, from Tromsø6 to Tromsø7, LVMi increased significantly more in Moderate compared to Low PA, with a mean group difference in LVMi enlargement of 3.9 g/m2.7 (95% CI 0.23–7.57, p = 0.037) (Table 3). No significant differences in LVMi change were observed between Hard and Low PA (p = 0.172) and Hard and Moderate PA (p = 1.000).

TABLE 3
www.frontiersin.org

Table 3. Longitudinal associations between cumulative physical activity and change in left ventricular mass index from baseline: The Tromsø Study 2007–2016.

In sex-stratified adjusted analysis (Table 3), LVMi in females increased significantly more in Moderate than in Low PA, with a mean difference in change of 5.6 g/m2.7 (95% CI 1.61–9.53, p = 0.002), and in Moderate than Hard PA, with a mean difference in LVMi enlargement of 4.1 g/m2.7 (95% CI 0.35–7.92, p = 0.027). No significant difference between Hard and Low PA (p=1.000) was observed. In males, no significant differences were observed (p = 0.224). In age-stratified adjusted analysis (Table 3), no significant differences were observed (p ≥ 0.182).

In analysis of the association between cumulative PA and change in LVDi, significant associations were observed in females only (Supplementary Table S4). LVDi increased significant more in Moderate (0.07 cm/m2 ± SE 0.03) than in Low PA (−0.06 cm/m2, SE 0.04), with a mean group difference of 0.13 cm/m2 (95% CI 0.03 to 0.24, p = 0.010). However, no significant differences in LVDi change were observed between Hard and Low PA (p = 0.087) and Hard and Moderate PA (p = 1.000).

Associations between cumulative PA and cross-sectional LVMi in Tromsø7 are presented in Figure 5. Significant associations between cumulative PA and LVDi were observed in females only. Moreover, similar trends in the association between cumulative PA and LVMi were observed in unadjusted, baseline adjusted, and in fully adjusted analysis.

FIGURE 5
www.frontiersin.org

Figure 5. Associations between cumulative PA and cross-sectional LV mass index (LVMi) in Tromsø7. (A) is unadjusted, (B) is adjusted for baseline LVMi in Tromsø6, (C) is adjusted for baseline LVMi in addition to age, sex, body mass index, and hypertension groups. Differences between groups of cumulative PA are indicated with p-values. Error bars indicate 95% CI. PA, physical activity; LV, left ventricle; CI, confidence interval.

Cumulative PA and Change in Cardiac Function From Tromsø6 to Tromsø7

The observed association observed between cumulative PA and change in LA/LV ratio overall (p = 0.075), stratified by sex (p ≥ 0.065), or stratified by age (p ≥ 0.083) was non-significant (Supplementary Table S5). No significant association was observed between cumulative PA and change in Mitral annular e' velocity overall (p = 0.903), stratified by sex (p ≥ 0.529), stratified by age (p ≥ 0.749), or stratified by hypertension (p ≥ 0.196) (Supplementary Table S6). No significant association was observed between cumulative PA and change in change in E/e' ratio overall (p = 0.253), stratified by sex (p ≥ 0.286), stratified by age (p ≥ 0.213), or stratified by body mass index (p ≥ 0.180) (Supplementary Table S7). No significant association was observed between cumulative PA and change in LV EF overall (p = 0.970), stratified by sex (p ≥ 0.652), or stratified by age (p ≥ 0.556) (Supplementary Table S8).

Sensitivity Analysis

When we stepwise, or jointly, excluded participants with known cardiac pathologies, we observed rather similar associations between cumulative PA and change in echocardiography measurements as in the fully adjusted model 2 (Supplementary Table S9). Furthermore, when smoking, alcohol consumption, diabetes, and LDL cholesterol were stepwise added to model 2, the associations between cumulative PA and change in LADi and between cumulative PA and change in LVMi did not change, except when diabetes was added to the model, the association between cumulative PA and LVMi was no longer significant (p = 0.068).

Discussion

Exercise-induced cardiac remodeling is well documented in athletes. Our longitudinal study adds to this knowledge by showing that more moderate levels of habitual PA over time is associated with cardiac remodeling also in a general adult and elderly population. The main finding from our study is that higher levels of cumulative PA was associated with increased LA size in males and in participants <65 years, and that moderate level of cumulative PA was associated with increased LV size in females.

Despite the association between cumulative PA and increased LA and LV sizes, indices of cardiac pump function and atrioventricular remodeling did not differ significantly between groups of cumulative PA. This may indicate that cardiac chamber enlargement is a physiological response to PA.

Cumulative PA and Increased LA and LV Sizes

In our study of the general population, we observed that Hard cumulative PA was associated with a larger increase in LADi than lower PA levels; although when stratified by sex or age, increased LADi was only observed in males and in participants <65 years. Furthermore, Moderate cumulative PA was associated with increased LVMi and LVDi, but only in females when stratified by sex or age.

Our observations are at large consistent with previous studies of athletes. Several meta-analyses have reported that LA and LV sizes are larger in endurance trained athletes compared to non-athletes or sedentary controls (9, 3032). Moreover, the relationship between endurance training and increased LV volume and mass has been demonstrated in a recent meta-analysis of both males and females (33). Additionally, the relationship between endurance training and increased LA volume, LV volume and LV mass has been confirmed in endurance trained young male and female athletes after 90 days of training (34). Similarly, increased LV volume and mass has been demonstrated in young sedentary males and females after 1 year of intensive endurance training (35).

Furthermore, the relationship between endurance training and enlarged LA volume and LV volume has been confirmed in middle-aged sedentary males and females after 10 months high-intensity endurance training (36); both LA and LV volumes increased significantly, but were considerably smaller when compared with a control group of age matched endurance athletes with a long history of endurance training (36). Additionally, a relationship between high levels of cumulative lifetime training hours and larger LA volume has been observed in males (37, 38), but no association between cumulative lifetime training hours and change in LV diameter or mass (38). Similarly, Mahjoub and colleagues demonstrated that LA volume increased after only 6 weeks of high-intensity endurance training in endurance trained men, whereas no change in LV mass, volume, or diameter was seen (39).

The findings from the previously discussed studies demonstrate that extensive LA and LV remodeling requires high amounts of endurance training stimuli over a long time. Similarly, our results indicate that the left atrium adapts faster to exercise than the left ventricle, and that sufficient and potentially higher stimulus from exercise intensity and volume is required for the left ventricle to remodel. The faster LA remodeling may be explained by the fact that the LA walls are thinner than the LV walls (11), and therefore are more affected by the hemodynamic overload during exercise according to the Laplace's law. In our study, the stimulus from moderate levels of habitual PA over time may have been insufficient to induce LV remodeling, which may explain the lack of association between cumulative PA and increased LV sizes in our study, except for females with Moderate PA. Furthermore, the lack of association between cumulative PA and change in LV size is supported by our sensitivity analysis, as the association between cumulative PA and change in LVMi became weaker and non-significant when we adjusted for diabetes.

Age and Sex Modifications

It is well documented that the prevalence of cardiovascular risk factors such as hypertension increase progressively with age, with a prevalence of 60% in participants ≥60 years (21). Untreated hypertension causes LV hypertrophy, which impairs LV relaxation and induces LV diastolic dysfunction and LA enlargement (21). Thus, the lack of increase in LADi in participants ≥65 years may be due to age related changes in the heart.

The observed sex differences in the association between cumulative PA and LA size may be explained by physiological and morphological differences between males and females (40). Females are on average smaller, have lower lean mass and a different sex hormone profile than males, which significantly impacts cardiac size (41). As females generally have smaller cardiac chambers than males (19), males exhibit more pronounced cardiac changes despite similar relative increase in chamber sizes (41). Finally, there may be quantitative and qualitative differences in exercise patterns between males and females (40). This is supported by accelerometry-measured data from the general adult and elderly population, where females accumulated more minutes of light PA and males accumulated more minutes of moderate and vigorous PA (42, 43).

Cumulative PA and Change in Cardiac Function

Despite the association between cumulative PA and increased LA and LV sizes, no significant differences in mitral annular e' velocity, E/e' ratio, LV EF, or LADi/LVDi ratio were observed between groups of cumulative PA. Thus, our results demonstrate that changes in indices of LV diastolic and systolic function, and atrioventricular chamber ratio, do not differ between groups of cumulative PA. The observed cardiac chamber enlargement with higher levels of cumulative PA in our study seems to be a physiological adaptation to exercise.

Our observations are consistent with previous reports of preserved cardiac function in athletes with exercise-induced cardiac remodeling. Studies of endurance athletes and elite soccer players have observed that LV diastolic function, as measured by Mitral valve and/or Tissue Doppler imaging, is preserved or even supranormal in athletes with cardiac chamber enlargement (13, 14, 38, 44). Also, studies have observed that LV systolic function, as measured by LV EF and/or LV fractional shortening, is normal in athletes with cardiac chamber enlargement (13, 15). Furthermore, preserved LV systolic function in athletes, as measured by LV EF and LV fractional shortening, has been confirmed in a meta-analysis of males and females at rest and during exercise (31). The authors observed no differences in LV systolic function between athletes and matched control subjects (31). Additionally, the effects of endurance training has been evaluated in a recent meta-analysis, where it was demonstrated that LV systolic function, as measured by LV EF and LV stroke volume, was slightly increased in males, but unaltered in females (33). In cross-sectional studies from the general population, no significant associations between increased LA volume and LV diastolic dysfunction, as measured by E/e' ratio, e', and/or tricuspid regurgitation velocity, was observed in physically active participants (45, 46).

In contrast, Lakatos and colleagues observed normal, but lower LV systolic function, as measured by LV EF and/or LV global longitudinal strain, in elite endurance athletes compared to non-athletes (47). Similarly, despite no difference in LV EF, it has been observed that LV global longitudinal strain was lower in elite endurance athletes than in non-athletes (13). With exercise-induced LV remodeling, it is possible that less myocardial deformation is required to obtain the same stroke volume. Therefore, reduced LV global longitudinal strain may be an adaptive change in elite endurance athletes (13).

Our observations of a balanced LADi/LVDi ratio, despite increased LA and LV sizes, is consistent with studies observing symmetrical enlargement of all four chambers (34), and that LA volume/LV volume ratio is similar despite LA enlargement in endurance athletes (13). An increased LA/LV ratio may be due to increased LV pressure and/or LV diastolic impairment, whereas an increased LA chamber with normal LA/LV ratio likely reflects a physiological adaptation to exercise (13).

In contrast to preserved pump function and balanced remodeling in the athlete's heart, increased risk of atrial fibrillation is seen in both adult and elderly endurance athletes (48, 49). It is suggested that LA enlargement itself may be a substrate for atrial fibrillation in athletes (50, 51), and therefore that the athlete's heart may potentially be proarrhythmic independent of other abnormalities. However, convincing data linking the combination of exercise and LA size to AF are lacking and are largely speculative (50, 52). Moreover, in a recent study investigating the acute effects of strenuous endurance exercise on atrial size and function in master athletes (53), the authors reported no exercise-induced atrial dysfunction or change in atrial size after an ultramarathon compared with baseline. Moreover, acute exercise-induced atrial fibrillation was uncommon during the race (53).

Strengths and Limitations

The main strength of our study is the longitudinal design with repeated measurements of PA and echocardiographic structural and functional data, which enables evaluation of the direction of the associations as well as change from baseline. Moreover, the broad diversity of covariates allowed us to adjust for multiple potential confounders.

Our study has several limitations that should be addressed. First, due to the observational nature of this study, causation cannot be established. Second, LADi, LVDi, and LV EF were assessed by linear measurements, which are less accurate and have more geometrically assumptions than the recommended biplane volume calculated parameters (19). However, in Tromsø7, we found moderate correlation between biplane-calculated EF and Teichholz-calculated EF (r = 0.42), and between LADi and LA volume index (r = 0.45). Furthermore, LVDi correlated strongly with LV volume index (r = 0.87). Third, our study lacks assessment of LA function which may distinguish between pathological and physiological remodeling (8). Fourth, self-reported PA is prone to both recall- and social desirability bias (54), and misclassifications would probably underestimate the true effects of PA. However, in a sub-study of Tromsø6, self-reported PA using the Saltin-Grimby Physical Activity Level Scale was significantly correlated with maximal oxygen uptake (females rs = 0.40, males rs = 0.44, both p < 0.001) (55). Moreover, there was a significant positive linear trend between maximal oxygen uptake and levels of self-reported PA (55). This is consistent with the sensitivity analysis of cumulative PA performed on our analytical sample (Supplementary Table S2). Fifth, we cannot exclude residual confounding by measured or unmeasured variables (e.g. masked hypertension or sex hormones). Finally, the relatively low sample size in our study represents a potential limitation. However, baseline characteristics did not differ between our analytical sample and the total cohort attending the first visit in Tromsø6 (n = 12,981), which strengthens our external validity to other Northern-European Caucasian adult populations.

In conclusion, higher levels of cumulative PA were associated with increased LADi in males and participants <65 years, and with increased LVMi and LVDi in females. Despite the association between cumulative PA and cardiac chamber enlargement, the function of the heart did not change with higher levels of PA, and the atrioventricular ratio was unchanged. This indicate that cardiac chamber enlargement is a physiological response to PA.

Data Availability Statement

The datasets presented in this article are not readily available because the legal restriction on data availability is set by the Tromsø Study Data and Publication Committee to control for data sharing, including publication of datasets with the potential of reverse identification of deidentified sensitive participant information. The data can however be made available from the Tromsø Study upon application to the Tromsø Study Data and Publication Committee. Requests to access the datasets should be directed to the Tromsø Study, Department of Community Medicine, Faculty of Health Sciences, UiT The Arctic University of Norway; e-mail: tromsous@uit.no.

Ethics Statement

The studies involving human participants were reviewed and approved by Regional Committee for Medical and Health Research Ethics, Tromsø, Norway (20828/REK Nord). The participants provided their written informed consent to participate in this study.

Author Contributions

KH, BW, and BM contributed to conception or design of the work. KH drafted the manuscript. All authors contributed to acquisition or analysis of the data. All authors contributed to interpretation of the data, critically revised the manuscript, gave final approval, and agree to be accountable for all aspects of work ensuring integrity and accuracy.

Funding

KH was supported by the Northern Norway Regional Health Authority (Grant Number HNF1406-18).

Conflict of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher's Note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

Acknowledgments

We thank the participants in the Tromsø Study for their contribution.

Supplementary Material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fcvm.2022.882077/full#supplementary-material

References

1. Pelliccia A, Caselli S, Sharma S, Basso C, Bax JJ, Corrado D, 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) 39:1949–69. doi: 10.1093/eurheartj/ehx532

PubMed Abstract | CrossRef Full Text | Google Scholar

2. Hoit BD. Left atrial size and function: role in prognosis. J Am Coll Cardiol. (2014) 63:493–505. doi: 10.1016/j.jacc.2013.10.055

PubMed Abstract | CrossRef Full Text | Google Scholar

3. Stylidis M, Sharashova E, Wilsgaard T, Leon DA, Heggelund G, Rösner A, et al. Left atrial diameter, left ventricle filling indices, and association with all-cause mortality: results from the population-based tromsø study. Echocardiography. (2019) 36:439–50. doi: 10.1111/echo.14270

PubMed Abstract | CrossRef Full Text | Google Scholar

4. Yildiz M, Oktay AA, Stewart MH, Milani RV, Ventura HO, Lavie CJ. Left ventricular hypertrophy and hypertension. Prog Cardiovasc Dis. (2020) 63:10–21. doi: 10.1016/j.pcad.2019.11.009

PubMed Abstract | CrossRef Full Text | Google Scholar

5. Chen YC, Voskoboinik A, Gerche A, Marwick TH, McMullen JR. Prevention of pathological atrial remodeling and atrial fibrillation: JACC state-of-the-art review. J Am Coll Cardiol. (2021) 77:2846–64. doi: 10.1016/j.jacc.2021.04.012

PubMed Abstract | CrossRef Full Text | Google Scholar

6. Baggish AL, Wood MJ. Athlete's heart and cardiovascular care of the athlete: scientific and clinical update. Circulation. (2011) 123:2723–35. doi: 10.1161/CIRCULATIONAHA.110.981571

PubMed Abstract | CrossRef Full Text | Google Scholar

7. D'Ascenzi F, Fiorentini C, Anselmi F, Mondillo S. Left ventricular hypertrophy in athletes: How to differentiate between hypertensive heart disease and athlete's heart. Eur J Prev Cardiol. (2020) 2047487320911850. doi: 10.1177/2047487320911850

PubMed Abstract | CrossRef Full Text | Google Scholar

8. D'Ascenzi F, Anselmi F, Focardi M, Mondillo S. Atrial enlargement in the athlete's heart: assessment of atrial function may help distinguish adaptive from pathologic remodeling. J Am Soc Echocardiogr. (2018) 31:148–57. doi: 10.1016/j.echo.2017.11.009

PubMed Abstract | CrossRef Full Text | Google Scholar

9. Iskandar A, Tokir Mujtaba MD, Thompson P. Left Atrium Size in Elite Athletes. JACC Cardiovasc Imaging. (2015) 8:753–62. doi: 10.1016/j.jcmg.2014.12.032

PubMed Abstract | CrossRef Full Text | Google Scholar

10. Pelliccia A, Maron BJ, Di Paolo FM, Biffi A, Quattrini FM, Pisicchio C, et al. Prevalence and clinical significance of left atrial remodeling in competitive athletes. J Am Coll Cardiol. (2005) 46:690–6. doi: 10.1016/j.jacc.2005.04.052

PubMed Abstract | CrossRef Full Text | Google Scholar

11. Gjerdalen G, Hisdal J, Solberg E, Andersen T, Radunovic Z, Steine K. Atrial Size and Function in Athletes. Int J Sports Med. (2015) 36:1170–6. doi: 10.1055/s-0035-1555780

PubMed Abstract | CrossRef Full Text | Google Scholar

12. McClean G, George K, Lord R, Utomi V, Jones N, Somauroo J, et al. Chronic adaptation of atrial structure and function in elite male athletes. Eur Heart J Cardiovasc Imaging. (2015) 16:417–22. doi: 10.1093/ehjci/jeu215

PubMed Abstract | CrossRef Full Text | Google Scholar

13. Trivedi SJ, Claessen G, Stefani L, Flannery MD, Brown P, Janssens K, et al. Differing mechanisms of atrial fibrillation in athletes and non-athletes: alterations in atrial structure and function. Eur Heart J Cardiovasc Imaging. (2020) 21:1374–83. doi: 10.1093/ehjci/jeaa183

PubMed Abstract | CrossRef Full Text | Google Scholar

14. Król W, Jedrzejewska I, Konopka M, Burkhard-Jagodzińska K, Klusiewicz A, Pokrywka A, et al. Left atrial enlargement in young high-level endurance athletes - another sign of athlete's heart? J Hum Kinet. (2016) 53:81–90. doi: 10.1515/hukin-2016-0012

PubMed Abstract | CrossRef Full Text | Google Scholar

15. Pelliccia A, Culasso F, Di Paolo FM, Maron BJ. Physiologic left ventricular cavity dilatation in elite athletes. Ann Intern Med. (1999) 130:23–31. doi: 10.7326/0003-4819-130-1-199901050-00005

PubMed Abstract | CrossRef Full Text | Google Scholar

16. Martinez MW, Kim JH, Shah AB, Phelan D, Emery MS, Wasfy MM, et al. Exercise-induced cardiovascular adaptations and approach to exercise and cardiovascular disease: JACC state-of-the-art review. J Am Coll Cardiol. (2021) 78:1453–70. doi: 10.1016/j.jacc.2021.08.003

PubMed Abstract | CrossRef Full Text | Google Scholar

17. Jacobsen BK, Eggen AE, Mathiesen EB, Wilsgaard T, Njølstad I. Cohort profile: the Tromso Study. Int J Epidemiol. (2012) 41:961–7. doi: 10.1093/ije/dyr049

PubMed Abstract | CrossRef Full Text | Google Scholar

18. Grimby G, Börjesson M, Jonsdottir IH, Schnohr P, Thelle DS, Saltin B. The “Saltin–Grimby Physical Activity Level Scale” and its application to health research. Scand J Med Sci Sports. (2015) 25:119–25. doi: 10.1111/sms.12611

PubMed Abstract | CrossRef Full Text | Google Scholar

19. Lang RM, Badano LP, Mor-Avi V, Afilalo J, Armstrong A, Ernande L, et al. Recommendations for cardiac chamber quantification by echocardiography in adults: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. J Am Soc Echocardiogr. (2015) 28:1–39.e14. doi: 10.1016/j.echo.2014.10.003

PubMed Abstract | CrossRef Full Text | Google Scholar

20. Du Bois D, Du Bois EF. A formula to estimate the approximate surface area if height and weight be known. 1916. Nutrition. (1989) 5:303–11; discussion 312–3.

PubMed Abstract | Google Scholar

21. Williams B, Mancia G, Spiering W, Agabiti Rosei E, Azizi M, Burnier M, et al. 2018 ESC/ESH guidelines for the management of arterial hypertension: the task force for the management of arterial hypertension of the European Society of Cardiology (ESC) and the European Society of Hypertension (ESH). Eur Heart J. (2018) 39:3021–104. doi: 10.1093/eurheartj/ehy339

PubMed Abstract | CrossRef Full Text | Google Scholar

22. Teichholz LE, Kreulen T, Herman MV, Gorlin R. Problems in echocardiographic volume determinations: echocardiographic-angiographic correlations in the presence of absence of asynergy. Am J Cardiol. (1976) 37:7–11. doi: 10.1016/0002-9149(76)90491-4

PubMed Abstract | CrossRef Full Text | Google Scholar

23. Nagueh SF, Smiseth OA, Appleton CP, Byrd BF. III, Dokainish H, Edvardsen T, et al. Recommendations for the evaluation of left ventricular diastolic function by echocardiography: an update from the American Society of Echocardiography and the European Association of Cardiovascular imaging. Eur Heart J Cardiovasc. (2016) 17:1321–60. doi: 10.1093/ehjci/jew082

PubMed Abstract | CrossRef Full Text | Google Scholar

24. Eveborn GW, Schirmer H, Heggelund G, Lunde P, Rasmussen K. The evolving epidemiology of valvular aortic stenosis. the Tromsø study. Heart. (2013) 99:396–400. doi: 10.1136/heartjnl-2012-302265

PubMed Abstract | CrossRef Full Text | Google Scholar

25. Zoghbi WA, Adams D, Bonow RO, Enriquez-Sarano M, Foster E, Grayburn PA, et al. Recommendations for noninvasive evaluation of native valvular regurgitation: a report from the American Society of Echocardiography developed in collaboration with the society for cardiovascular magnetic resonance. J Am Soc Echocardiogr. (2017) 30:303–71. doi: 10.1016/j.echo.2017.01.007

PubMed Abstract | CrossRef Full Text | Google Scholar

26. Bonow RO, Carabello BA, Chatterjee K, de Leon AC Jr., Faxon DP, Freed MD, et al. 2008 Focused update incorporated into the ACC/AHA 2006 guidelines for the management of patients with valvular heart disease: a report of the American College of Cardiology/American Heart Association task force on practice guidelines (writing committee to revise the (1998) guidelines for the management of patients with valvular heart disease): endorsed by the Society of Cardiovascular Anesthesiologists, Society for Cardiovascular Angiography and Interventions, and Society of Thoracic Surgeons. Circulation. (2008) 118:e523–661. doi: 10.1161/CIRCULATIONAHA.108.190748

PubMed Abstract | CrossRef Full Text | Google Scholar

27. Stylidis M, Leon DA, Rösner A, Schirmer H. Global myocardial longitudinal strain in a general population—associations with blood pressure and subclinical heart failure: the Tromsø Study. Int J Cardiovasc Imaging. (2020) 36:459–70. doi: 10.1007/s10554-019-01741-3

PubMed Abstract | CrossRef Full Text | Google Scholar

28. Eggen AE, Mathiesen EB, Wilsgaard T, Jacobsen BK, Njølstad I. The sixth survey of the Tromso Study (Tromso 6) in 2007-08: collaborative research in the interface between clinical medicine and epidemiology: study objectives, design, data collection procedures, and attendance in a multipurpose population-based health survey. Scand J Public Health. (2013) 41:65–80. doi: 10.1177/1403494812469851

PubMed Abstract | CrossRef Full Text | Google Scholar

29. Nyrnes A, Mathiesen EB, Njølstad I, Wilsgaard T, Løchen ML. Palpitations are predictive of future atrial fibrillation. An 11-year follow-up of 22,815 men and women: the Tromsø study. Eur J Prev Cardiol. (2013) 20:729–36. doi: 10.1177/2047487312446562

PubMed Abstract | CrossRef Full Text | Google Scholar

30. Cuspidi C, Sala C, Tadic M, Baccanelli G, Gherbesi E, Grassi G, et al. Left atrial volume in elite athletes: a meta-analysis of echocardiographic studies. Scand J Med Sci Sports. (2019) 29:922–32. doi: 10.1111/sms.13416

PubMed Abstract | CrossRef Full Text | Google Scholar

31. Fagard R. Athlete's heart. Heart. (2003) 89:1455–61. doi: 10.1136/heart.89.12.1455

PubMed Abstract | CrossRef Full Text | Google Scholar

32. Utomi V, Oxborough D, Whyte GP, Somauroo J, Sharma S, Shave R, et al. Systematic review and meta-analysis of training mode, imaging modality and body size influences on the morphology and function of the male athlete's heart. Heart. (2013) 99:1727–33. doi: 10.1136/heartjnl-2012-303465

PubMed Abstract | CrossRef Full Text | Google Scholar

33. Diaz-Canestro C, Montero D. The impact of sex on left ventricular cardiac adaptations to endurance training: a systematic review and meta-analysis. Sports Med. (2020) 50:1501–13. doi: 10.1007/s40279-020-01294-9

PubMed Abstract | CrossRef Full Text | Google Scholar

34. Baggish AL, Wang F, Weiner RB, Elinoff JM, Tournoux F, Boland A, et al. Training-specific changes in cardiac structure and function: a prospective and longitudinal assessment of competitive athletes. J Appl Physiol. (2008) 104:1121–8. doi: 10.1152/japplphysiol.01170.2007

PubMed Abstract | CrossRef Full Text | Google Scholar

35. Arbab-Zadeh A, Perhonen M, Howden E, Peshock Ronald M, Zhang R, Adams-Huet B, et al. Cardiac remodeling in response to 1 year of intensive endurance training. Circulation. (2014) 130:2152–61. doi: 10.1161/CIRCULATIONAHA.114.010775

PubMed Abstract | CrossRef Full Text | Google Scholar

36. Opondo MA, Aiad N, Cain MA, Sarma S, Howden E, Stoller DA, et al. Does high-intensity endurance training increase the risk of atrial fibrillation? A longitudinal study of left atrial structure and function. Circ Arrhythm Electrophysiol. (2018) 11:e005598. doi: 10.1161/CIRCEP.117.005598

PubMed Abstract | CrossRef Full Text | Google Scholar

37. Diaz Babio G, Vera Janavel G, Constantin I, Masson G, Carrero C, Garcia Botta T, et al. Atrial size and sports. A great training for a greater left atrium: how much is too much? Int J Cardiovasc Imaging. (2021) 37:981–8. doi: 10.1007/s10554-020-02082-2

PubMed Abstract | CrossRef Full Text | Google Scholar

38. Elliott AD, Mahajan R, Linz D, Stokes M, Verdicchio CV, Middeldorp ME, et al. Atrial remodeling and ectopic burden in recreational athletes: implications for risk of atrial fibrillation. Clin Cardiol. (2018) 41:843–8. doi: 10.1002/clc.22967

PubMed Abstract | CrossRef Full Text | Google Scholar

39. Mahjoub H, Le Blanc O, Paquette M, Imhoff S, Labrecque L, Drapeau A, et al. Cardiac remodeling after six weeks of high-intensity interval training to exhaustion in endurance-trained men. Am J Physiol Heart Circ Physiol. (2019) 317:H685–h94. doi: 10.1152/ajpheart.00196.2019

PubMed Abstract | CrossRef Full Text | Google Scholar

40. Finocchiaro G, Dhutia H, D'Silva A, Malhotra A, Steriotis A, Millar L, et al. Effect of sex and sporting discipline on LV adaptation to exercise. JACC Cardiovasc imaging. (2017) 10:965–72. doi: 10.1016/j.jcmg.2016.08.011

PubMed Abstract | CrossRef Full Text | Google Scholar

41. Finocchiaro G, Sharma S. Do endurance sports affect female hearts differently to male hearts? Future Cardiol. (2016) 12:105–8. doi: 10.2217/fca.15.85

PubMed Abstract | CrossRef Full Text | Google Scholar

42. Sagelv EH, Ekelund U, Pedersen S, Brage S, Hansen BH, Johansson J, et al. Physical activity levels in adults and elderly from triaxial and uniaxial accelerometry. The Tromsø Study. PloS ONE. (2019) 14:e0225670. doi: 10.1371/journal.pone.0225670

PubMed Abstract | CrossRef Full Text | Google Scholar

43. Baptista F, Santos DA, Silva AM, Mota J, Santos R, Vale S, et al. Prevalence of the portuguese population attaining sufficient physical activity. Med Sci Sports Exerc. (2012) 44:466–73. doi: 10.1249/MSS.0b013e318230e441

PubMed Abstract | CrossRef Full Text | Google Scholar

44. D'Ascenzi F, Cameli M, Zacà V, Lisi M, Santoro A, Causarano A, et al. Supernormal diastolic function and role of left atrial myocardial deformation analysis by 2D speckle tracking echocardiography in elite soccer players. Echocardiography. (2011) 28:320–6. doi: 10.1111/j.1540-8175.2010.01338.x

PubMed Abstract | CrossRef Full Text | Google Scholar

45. Heitmann KA, Løchen M-L, Hopstock LA, Stylidis M, Welde B, Schirmer H, et al. Cross-sectional associations between accelerometry-measured physical activity, left atrial size, and indices of left ventricular diastolic dysfunction: The Tromsø Study. Prev Med Rep. (2021) 21:101290. doi: 10.1016/j.pmedr.2020.101290

PubMed Abstract | CrossRef Full Text | Google Scholar

46. Letnes JM, Nes B, Vaardal-Lunde K, Slette MB, Mølmen-Hansen HE, Aspenes ST, et al. Left atrial volume, cardiorespiratory fitness, and diastolic function in healthy individuals: the HUNT study, Norway. J Am Heart Assoc. (2020) 9:e014682. doi: 10.1161/JAHA.119.014682

PubMed Abstract | CrossRef Full Text | Google Scholar

47. Lakatos BK, Molnár A, Kiss O, Sydó N, Tokodi M, Solymossi B, et al. Relationship between cardiac remodeling and exercise capacity in elite athletes: incremental value of left atrial morphology and function assessed by three-dimensional echocardiography. J Am Soc Echocardiogr. (2020) 33:101–9.e1. doi: 10.1016/j.echo.2019.07.017

PubMed Abstract | CrossRef Full Text | Google Scholar

48. Andersen K, Farahmand B, Ahlbom A, Held C, Ljunghall S, Michaëlsson K, et al. Risk of arrhythmias in 52 755 long-distance cross-country skiers: a cohort study. Eur Heart J. (2013) 34:3624–31. doi: 10.1093/eurheartj/eht188

PubMed Abstract | CrossRef Full Text | Google Scholar

49. Abdulla J, Nielsen JR. Is the risk of atrial fibrillation higher in athletes than in the general population? A systematic review and meta-analysis. Europace. (2009) 11:1156–9. doi: 10.1093/europace/eup197

PubMed Abstract | CrossRef Full Text | Google Scholar

50. Sanchis-Gomar F, Perez-Quilis C, Lippi G, Cervellin G, Leischik R, Löllgen H, et al. Atrial fibrillation in highly trained endurance athletes - description of a syndrome. Int J Cardiol. (2017) 226:11–20. doi: 10.1016/j.ijcard.2016.10.047

PubMed Abstract | CrossRef Full Text | Google Scholar

51. Morseth B, Løchen M-L, Ariansen I, Myrstad M, Thelle DS. The ambiguity of physical activity, exercise and atrial fibrillation. Eur J Prev Cardiol. (2018) 25:624–36. doi: 10.1177/2047487318754930

PubMed Abstract | CrossRef Full Text | Google Scholar

52. D'Ascenzi F, Cameli M, Ciccone MM, Maiello M, Modesti PA, Mondillo S, et al. The controversial relationship between exercise and atrial fibrillation: clinical studies and pathophysiological mechanisms. J Cardiovasc Med (Hagerstown). (2015) 16:802–10. doi: 10.2459/JCM.0000000000000211

PubMed Abstract | CrossRef Full Text | Google Scholar

53. Cavigli L, Zorzi A, Spadotto V, Mandoli GE, Melani A, Fusi C, et al. The acute effects of an ultramarathon on atrial function and supraventricular arrhythmias in master athletes. J Clin Med. (2022) 11:528. doi: 10.3390/jcm11030528

PubMed Abstract | CrossRef Full Text | Google Scholar

54. Prince SA, Adamo KB, Hamel ME, Hardt J, Gorber SC, Tremblay M, et al. comparison of direct versus self-report measures for assessing physical activity in adults: a systematic review. Int J Behav Nutr Phys Act. (2008) 5:56. doi: 10.1186/1479-5868-5-56

PubMed Abstract | CrossRef Full Text | Google Scholar

55. Emaus A, Degerstrøm J, Wilsgaard T, Hansen BH, Dieli-Conwright CM, Furberg AS, et al. Does a variation in self-reported physical activity reflect variation in objectively measured physical activity, resting heart rate, and physical fitness? Results from the Tromso study. Scand J Public Health. (2010) 38(Suppl. 5):105–18. doi: 10.1177/1403494810378919

PubMed Abstract | CrossRef Full Text | Google Scholar

Keywords: athlete's heart, cardiac, echocardiography, ejection fraction, exercise, left atrium, left ventricle, public health

Citation: Heitmann KA, Welde B, Løchen M-L, Stylidis M, Schirmer H and Morseth B (2022) Longitudinal Associations Between Cumulative Physical Activity and Change in Structure and Function of the Left Side of the Heart: The Tromsø Study 2007–2016. Front. Cardiovasc. Med. 9:882077. doi: 10.3389/fcvm.2022.882077

Received: 23 February 2022; Accepted: 13 April 2022;
Published: 12 May 2022.

Edited by:

Flavio D'Ascenzi, University of Siena, Italy

Reviewed by:

Luna Cavigli, University of Siena, Italy
Marco Matteo Ciccone, University of Bari Aldo Moro, Italy

Copyright © 2022 Heitmann, Welde, Løchen, Stylidis, Schirmer and Morseth. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Kim Arne Heitmann, kim.a.heitmann@uit.no