Atrial Enlargement in the Athlete’s Heart: Assessment of Atrial Function May Help Distinguish Adaptive from Pathologic Remodeling




Intensive training is associated with hemodynamic changes that typically induce an enlargement of cardiac chambers, involving not only the ventricles but also the atria. The hearts of competitive athletes are characterized by increases in left and right atrial dimensions that have been interpreted as a physiologic adaptation to training. Conversely, some authors have hypothesized maladaptive remodeling; furthermore, the extent of left atrial dimensional remodeling may overlap atrial dilation observed in patients with cardiac disease, representing a challenge for clinicians. However, studies investigating left and right atrial function in athletes have demonstrated that atrial size is insufficient to provide mechanistic information about the atrium itself, and an increase in atrial size is not intrinsically an expression of atrial dysfunction. The authors critically analyze training-induced atrial remodeling, taking into account not only the assessment of atrial size but also the evaluation of atrial function, suggesting that the characterization of atrial function plays a fundamental role in the evaluation of athlete’s heart, being useful to differentiate physiologic remodeling induced by exercise from pathologic changes occurring in cardiac disorders.


Highlights





  • Atrial size is often increased in competitive athletes.



  • In athletes, atrial size can overlap atrial dilation observed in cardiac patients.



  • In athletes, atrial dilation is not intrinsically an expression of atrial dysfunction.



  • A reduction in reservoir function should raise the suspicion of a cardiac disorder.



  • Both atrial size and function should be assessed to distinguish physiology from pathology.



Intensive training leads to hemodynamic changes, including increases in cardiac output and stroke volume associated with the increase in maximal oxygen consumption during exercise. These changes typically induce an enlargement of cardiac chambers, involving not only the ventricles but also the atria. Unfortunately, exercise-induced remodeling of the right and left ventricles can mimic the dilation found in cardiac diseases such as dilated and/or arrhythmogenic cardiomyopathy. Furthermore, also atrial remodeling can represent a challenge in evaluating athlete’s heart due to similarities in terms of atrial size between athlete’s heart and cardiomyopathies such as hypertrophic and dilated cardiomyopathy. The availability of new cross-sectional and longitudinal data on left atrial (LA) and right atrial (RA) dimensional remodeling and the application of novel echocardiographic techniques to the characterization of atrial function have currently improved our understanding of physiologic remodeling induced by exercise and have provided useful information for the clinical characterization of athlete’s heart and differential diagnosis with cardiomyopathies. In this review we discuss the most relevant studies characterizing atrial size and function in athletes with a critical comparison with pathologic conditions. Published data suggest that the evaluation of atrial and ventricular function may be useful in distinguishing physiologic cardiac chamber enlargement induced by training from the dilation found in heart disease.


LA Size in Athlete’s Heart


In 2005, Pelliccia et al. , in a large population of 1,777 competitive athletes, found that 18% of competitive athletes had mild increases of left atrial (LA) anteroposterior diameter (≥40 mm), while 2% showed marked LA enlargement (≥45 mm). This increase in LA size was interpreted as a benign adaptation to the cardiac remodeling induced by training. The left atrium is not a symmetrically shaped three-dimensional structure, and measurement of LA volume reflects LA enlargement more precisely than anteroposterior diameter, which tends to underestimate LA size. Therefore, in 2010 D’Andrea et al. performed a study in athletes estimating LA size by two-dimensional volume indexed to body surface area. Comparing data from the athletic population to the previously established reference values, they found mild enlargement (defined as LA volume index between 29 and 33 mL/m 2 ) in 24% of the population and moderate enlargement (defined as LA volume index ≥ 34 mL/m 2 ) in 3.2%. Notably, according to the current recommendations that identified a new upper limit of 34 mL/m 2 for the definition of “atrial enlargement,” most of the athletes would be currently defined as having normal LA size.


In a recent meta-analysis of 54 studies comprising 7,189 elite athletes and 1,375 control subjects, Iskandar et al. confirmed that athletes had greater LA size in comparison with control subjects, with a 13% increase in LA diameter and a 30% increase in LA volume index. Mean LA diameter was 36.0 mm in male elite athletes and 34.2 mm in female elite athletes, and the overall mean diameter was 4.1 mm greater in comparison with sedentary control subjects ( P < .0001). Mean LA volume index in male elite athletes was 30.8 mL/m 2 , 7 mL/m 2 greater than in the sedentary population ( P < .01). Unfortunately, the small number of studies reporting this measurement in female athletes precluded a subgroup analysis for women. Notably, the upper limit for LA volume index in male athletes was 35.8 mL/m 2 and was greater than the established normal value (i.e., ≥34 mL/m 2 ), resulting in mild dilation according to the current recommendations established for the general population.


The LA response to the training stimulus is dynamic, and the extent of LA adaptation in athletes changes during the training period. Indeed, in a population of adolescent soccer players, an increase in LA volume index occurred after 4 months of intensive training, with a further increase after 8 months. Similar results were found by Baggish et al. , who reported an increase in LA volumes in endurance athletes after 90 days of team training. Conversely, LA dimensions did not significantly change after 90 days in strength-trained athletes. Dynamic remodeling of the left atrium was found through longitudinal studies also in adult soccer players and in female athletes, confirming that the left atrium rapidly adapts to different training loads, is dynamic, and can be reversed after a detraining period.


The characterization of atrial dimensions in athletes has improved through the assessment of LA volume using cardiac magnetic resonance, which provides high-quality images, is intrinsically three-dimensional, and does not rely on geometric assumptions, enabling more accurate morphologic analyses than echocardiography. The few cardiac magnetic resonance studies currently available confirm an increased LA volume index in athletes, particularly in those practicing endurance sports.


Although LA remodeling has been extensively investigated in adult athletes, few studies have been performed in children practicing sports. Triposkiadis et al. observed greater LA maximal and minimal volume in prepubertal swimmers compared with sedentary control. Greater LA dimensions were found also in football players. Krol et al. examined 117 young elite rowers and found that LA enlargement was present in nearly half of the athletes (43%), being more frequent in men than in women (52.5% vs 32.1%), with only 4.4% of athletes presenting severe enlargement. In a longitudinal study enrolling adolescent soccer players, it was found that during the competitive season, LA volume increased in response to changes in loading conditions. These results were further confirmed in a population of prepubertal competitive swimmers; indeed, after 5 months of intense training, LA volume indexes (assessed by two- and three-dimensional echocardiography) significantly increased, and a correlation between change in atrial volumes and change in stroke volume was found. These findings suggest that intensive training affects the growing hearts of young athletes with an additive increase in atrial size, suggesting that morphologic adaptations can occur also in the early phases of the career of an athlete.


Taken together, the current evidence suggests that atrial enlargement observed in athletes represents an adaptive mechanism to the increased volume overload induced by training. It is dynamic and reversible. However, in highly trained athletes, the extent of LA dimensional remodeling may be relevant, and absolute LA size can overlap atrial dilation observed in patients with cardiac disease, representing a challenge for clinicians in terms of differential diagnosis.




RA Size in Athlete’s Heart


Exercise-induced cardiac remodeling is not a prerogative of the left heart. Hemodynamic changes induced by long-term intensive training typically involve both left and right chambers, in a global and symmetric process. The right heart is known to be very sensitive to volume overload because of its thin wall, and although it is susceptible to elevated afterload, it tolerates better an increase in preload, which is able to alter the geometry of right heart but not to influence the pattern of ejection. However, the complex anatomy and the nonconcentric contraction of the right chambers have discouraged the echocardiographic quantitative assessment of the right heart, including the right atrium. To date, only a few studies have focused on the quantification of RA size.


In 2013, D’Andrea et al. studied a population of 650 athletes, with the aim of evaluating the impact of training on RA dimensions, defined by major and minor diameters and end-systolic area. Right heart measurements were significantly greater in endurance athletes than in age- and sex-matched strength athletes and control subjects. In agreement with these findings, elite athletes have greater RA dimensions compared with sedentary control subjects, and assessing RA size through RA volume, it was demonstrated that RA size is significantly increased in athletes even when RA volume is indexed to body surface area. Similar to the left atrium, the right atrium is able to rapidly adapt to the stimulus of training; indeed, in a population of female athletes, after 16 weeks of intensive training, RA area and RA volume index were significantly increased, supporting a cause-effect relationship between exercise and RA remodeling.


To standardize right cardiac measurements in athletes, Zaidi et al. suggested reference values for right heart dimensions, with upper limits for RA area of 28 cm 2 in male athletes and 24 cm 2 in female athletes and upper limits for RA index of 14 cm 2 /m 2 in male athletes and 13 cm 2 /m 2 in female athletes. Zaidi et al. found no significant differences between black and white male athletes but greater RA dimensions in white female athletes ( P < .001). Recently, Gjerdalen et al. found in 595 football players that 4.6% exceeded the previously suggested upper limit of 28 cm 2 , while 4.7% exceeded the suggested upper limit of 14 cm 2 /m 2 . Accordingly, they proposed a higher upper limit of 14.5 cm 2 /m 2 for RA area index and 2.9 cm/m 2 for RA minor axis. In a population of 1,009 Olympic athletes, the upper limits of RA area were 25 cm 2 for men and 20 cm 2 for women. A recent meta-analysis of 46 echocardiographic studies and 6,806 athletes confirmed that the upper limit of RA area in athletes was larger than that found in the general population. In particular, an upper value of 23 cm 2 for RA area may be applied as a normal criterion in the evaluation of athletes’ RA dimensions, exceeding the upper limit established for the general population (i.e., 18 cm 2 ).


Therefore, the present findings suggest that the right atrium physiologically adapts to the hemodynamic changes induced by exercise, similarly to the remodeling observed for the left atrium, with an increase in its size that is significantly different from the general population.




RA Size in Athlete’s Heart


Exercise-induced cardiac remodeling is not a prerogative of the left heart. Hemodynamic changes induced by long-term intensive training typically involve both left and right chambers, in a global and symmetric process. The right heart is known to be very sensitive to volume overload because of its thin wall, and although it is susceptible to elevated afterload, it tolerates better an increase in preload, which is able to alter the geometry of right heart but not to influence the pattern of ejection. However, the complex anatomy and the nonconcentric contraction of the right chambers have discouraged the echocardiographic quantitative assessment of the right heart, including the right atrium. To date, only a few studies have focused on the quantification of RA size.


In 2013, D’Andrea et al. studied a population of 650 athletes, with the aim of evaluating the impact of training on RA dimensions, defined by major and minor diameters and end-systolic area. Right heart measurements were significantly greater in endurance athletes than in age- and sex-matched strength athletes and control subjects. In agreement with these findings, elite athletes have greater RA dimensions compared with sedentary control subjects, and assessing RA size through RA volume, it was demonstrated that RA size is significantly increased in athletes even when RA volume is indexed to body surface area. Similar to the left atrium, the right atrium is able to rapidly adapt to the stimulus of training; indeed, in a population of female athletes, after 16 weeks of intensive training, RA area and RA volume index were significantly increased, supporting a cause-effect relationship between exercise and RA remodeling.


To standardize right cardiac measurements in athletes, Zaidi et al. suggested reference values for right heart dimensions, with upper limits for RA area of 28 cm 2 in male athletes and 24 cm 2 in female athletes and upper limits for RA index of 14 cm 2 /m 2 in male athletes and 13 cm 2 /m 2 in female athletes. Zaidi et al. found no significant differences between black and white male athletes but greater RA dimensions in white female athletes ( P < .001). Recently, Gjerdalen et al. found in 595 football players that 4.6% exceeded the previously suggested upper limit of 28 cm 2 , while 4.7% exceeded the suggested upper limit of 14 cm 2 /m 2 . Accordingly, they proposed a higher upper limit of 14.5 cm 2 /m 2 for RA area index and 2.9 cm/m 2 for RA minor axis. In a population of 1,009 Olympic athletes, the upper limits of RA area were 25 cm 2 for men and 20 cm 2 for women. A recent meta-analysis of 46 echocardiographic studies and 6,806 athletes confirmed that the upper limit of RA area in athletes was larger than that found in the general population. In particular, an upper value of 23 cm 2 for RA area may be applied as a normal criterion in the evaluation of athletes’ RA dimensions, exceeding the upper limit established for the general population (i.e., 18 cm 2 ).


Therefore, the present findings suggest that the right atrium physiologically adapts to the hemodynamic changes induced by exercise, similarly to the remodeling observed for the left atrium, with an increase in its size that is significantly different from the general population.




LA and RA Function: The Use of Novel Echocardiographic Techniques to Characterize Atrial Deformation


Atrial size is insufficient to provide mechanistic information about the atrium itself, and an increase in atrial size is not intrinsically an expression of atrial dysfunction. Therefore, the evaluation of atrial function plays a fundamental role in the assessment of athlete’s heart, and a clear understanding of atrial function, and particularly atrial reservoir function, may be useful to differentiate physiologic remodeling induced by exercise from pathologic changes occurring in cardiac disorders.


Several modalities, such as nuclear scintigraphy, angiography, and atrial pressure-volume loops, have been used to assess LA performance by measuring changes in LA volume over time. However, these methods are cumbersome, time consuming, and difficult to apply. Among the current techniques to estimate LA function, the volumetric estimation of LA phasic volumes obtained from maximum, minimum, and pre-P volumes by two-dimensional echocardiography is able to characterize the three phases of LA contribution to ventricular filling: during ventricular systole, when the left atrium acts as a “reservoir,” receiving blood from the pulmonary veins; during early diastole, when the left atrium operates as a “conduit,” transferring blood from the pulmonary veins into the left ventricle; and during late diastole, when the left atrium actively contracts to pump blood into the left ventricular (LV) cavity. The application of this echocardiographic technique to athlete’s heart has demonstrated that the atrial cavity responds to the exercise-induced increase in preload by enhancing reservoir and conduit function; this phenomenon is likely related to the need to accommodate the increasing venous return and maintain normal contractile function, efficient emptying function, and stroke volume. This adaptation is accompanied by an improvement in the diastolic properties of left and right ventricles, compared with normal subjects, particularly in athletes practicing endurance sports. Assessing LA function by phasic volumes in a cohort of soccer players, greater LA reservoir and conduit volumes were found in athletes compared with control subjects and similar LA active volumes. LA reservoir and conduit fractions were not significantly different between the groups; however, LA active emptying fraction was lower in athletes than control subjects. Moreover, the cohort of soccer players was longitudinally evaluated during the training period, observing that LA reservoir and conduit volume further increased with changes in volume and intensity of training, being greater at the end of the season compared with preseason data. LA active contractile phase did not change during the training period, showing that despite LA remodeling, the pump function remains preserved. Notably, in this study, despite the changes in LA volumes, the index of intracardiac filling pressure (i.e., the E/e′ ratio) was normal and remained within the normal range over the competitive season, further supporting the hypothesis that LA enlargement is physiologically induced by volume rather than pressure overload.


The estimation of atrial function can be obtained also by atrial ejection fraction by two- or three-dimensional echocardiography. This technique is feasible in both young and adult athletes. It has been demonstrated that LA ejection fraction does not differ between athletes and healthy control subjects, and it remains unchanged after 5 months of training in preadolescent athletes. Unfortunately, the use of these measures is limited mainly by the current lack of normative reference values. However, further studies collecting new data on athlete’s heart are warranted to derive normative reference values of atrial ejection fraction to be applied in athlete’s heart.


Also the estimation of peak systolic velocity (S) and systolic velocity-time integral of pulmonary venous (PV) systolic flow can be considered as indices of LA reservoir function. The evaluation of PV flow by pulsed Doppler echocardiography is a reliable and practical noninvasive method for detecting abnormalities of diastolic function. Although PV flow can be easily measured in clinical practice, this method has some limitations, such as the dependence of PV flow on variables such as age and preload. Furthermore, few and conflicting data have been collected with the application of this technique in athlete’s heart. Indeed, whereas some authors demonstrated a similar pattern of PV flow between athletes and control subjects, others observed an enhancement of conduit function in athletes assessed by PV early diastolic wave. Accordingly, this method is currently not routinely applied. However, further studies estimating PV systolic flow in large cohorts of athletes could provide relevant insights into the characterization of diastolic and LA reservoir function.


Recently, advanced echocardiographic techniques have begun to clarify significant functional adaptations of the myocardium that accompany previously reported morphologic features of athlete’s heart. In particular, speckle-tracking echocardiography (STE) has recently provided further insight into the characterization of atrial and ventricular myocardial properties of athletes.


STE is a noninvasive imaging technique that allows an objective and quantitative evaluation of global and regional myocardial function. STE-based analysis of myocardial contraction allows the quantification of fiber deformation through virtually any plane of the space, regardless to the imaging plane. In particular, myocardial strain is a dimensionless parameter expressed as the percentage of myocardial deformation. STE was originally applied to the left ventricle and then to left and right atria. The application of STE to the atria generates longitudinal strain curves for each segment, and a mean curve representing all the segments analyzed is obtained. Two different methods have been described for obtaining atrial strain curves: the first uses QRS onset on the electrocardiogram as the reference point for the generation of strain curves, while the second uses the P wave as the reference point. Each method has advantages and disadvantages, but taking into account the pros and cons of both methods, there is no definitive evidence for supporting either the P-wave or the QRS method to set the zero reference to measure atrial strain. We report in Figure 1 the QRS method, the most widely applied method in athlete’s heart to obtain LA and RA strain values. The application of the QRS method to the atria allows the generation of a mean curve that presents a positive peak at the end of the reservoir phase, defined as peak atrial longitudinal strain (PALS), a plateau corresponding to the phase of diastasis and a measure of atrial reservoir function, and a second positive peak just before atrial contraction, defined as peak atrial contraction strain (PACS), a measure of atrial contractile function. These parameters have been extensively investigated for the left atrium, and in normal subjects a recent meta-analysis suggested a normal reference range for LA reservoir strain of 39% (95% CI, 38%–41%) and for contractile strain of 17% (95% CI, 16%–19%). For the right atrium, a value for RA reservoir strain of 49 ± 13% was found to be normal in healthy subjects.




Figure 1


Application of STE to the left atrium of a control subject. As described in the text, two parameters can be obtained: PALS, a measure of atrial reservoir function, and PACS, a measure of atrial contractile function. This echocardiographic technique can be applied also to the right atrium. AVC , aortic valve closure.


The application of STE to the right and left atrium in athletes demonstrated a characteristic deformation of atrial myocardium in response to training. The first study applying STE to the left atrium in athletes was published in 2011 by our research group. We found that although reservoir function (i.e., PALS) did not differ between athletes and control subjects ( P = .33), LA active function (i.e., PACS) was lower in the former ( P < .0001). This finding was accompanied by supernormal diastolic function and was related to a shift of LV filling toward early diastole in athlete’s heart.


Recently, a new echocardiographic method to noninvasively derive the stiffness index was applied to athlete’s heart, using the E/e′ ratio and PALS. Using this index, it was demonstrated that despite greater LA size, athletes have a lower stiffness index in comparison with control subjects, demonstrating preserved compliance of the left atrium when the increase in atrial size is physiologically induced by exercise. STE has been used in athletes also to characterize RA deformation. Both PALS and PACS were found to be slightly reduced in athletes compared with control subjects, and this reduction was accompanied by a better diastolic function in the former and normal filling pressures, estimated by the E/e′ ratio. Pagourelias et al. applied STE to the right atrium in a cohort of 108 athletes (80 endurance- and 28 strength-trained athletes), reporting similar values and confirming that in athletes, despite enlargement of the right atrium, functional properties remain normal, contributing through atrioventricular coupling to preload increase and stroke volume augmentation. The estimation of RA stiffness by STE confirmed that despite an exercise-induced increase in atrial size, in competitive athletes RA myocardial stiffness is normal, as observed for the left atrium.


These studies demonstrated that the atria of athletes had a characteristic adaptation to training that goes beyond mere cavity enlargement. This morphofunctional adaptation is dynamic in its nature. Indeed, changes in both LA size and function during the competitive season were described in a cohort of soccer players, in whom decreases in global PALS and PACS after 4 and 8 months of training were found. However, this reduction was clinically not significant, also considering that both PALS and PACS were within the normal range at peak training. Reductions in LA and RA PALS and PACS after 16 weeks of intensive training were confirmed also in female athletes, but a stable PALS/PACS ratio with a balanced reduction of both PALS and PACS suggested a potentially benign remodeling.


A slight reduction in LA PALS with a typical reduction in contractile function was found after 5 months of intensive endurance training also in children, confirming the findings observed in adult athletes. However, in agreement with previous studies, despite this reduction, LA reservoir function was within normal values. Indeed, a dysfunction of atrial reservoir properties is uncommon in athletes, as confirmed also by Krol et al. , demonstrating in a population of young elite rowers that reduced LA PALS was present in <4% of athletes. Longitudinal studies with long-term follow-up are currently not available, and we cannot definitively confirm the benign nature of this adaptation. However, this slight decrease in LA reservoir function, measured by STE, is accompanied by common and physiologic adaptations of the heart, such as resting bradycardia, correlating with atrial volumes and with better ventricular performance. Therefore, these findings support the hypothesis of a benign adaptation of the atria to the supernormal performance of the ventricles at rest with a reserve that may be used during effort.


The current evidence suggests that the increases in LA and RA size are accompanied by normal reservoir function. The application of novel echocardiographic techniques to the assessment of atrial function in athlete’s heart allowed better characterization of myocardial deformation of the atria, confirming that atrial enlargement is not intrinsically an expression of atrial dysfunction and suggesting that the evaluation of atrial function should play a fundamental role in the assessment of athlete’s heart.

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Apr 15, 2018 | Posted by in CARDIOLOGY | Comments Off on Atrial Enlargement in the Athlete’s Heart: Assessment of Atrial Function May Help Distinguish Adaptive from Pathologic Remodeling

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