The impact of demographic, anthropometric and athletic characteristics on left atrial size in athletes

Abstract The structural adaptations of the “athlete's heart” include left atrial (LA) enlargement. A literature search was performed based on PubMed listings up to November 2, 2019 using “athletes AND left atrium,” “athletes AND LA,” “sports AND left atrium,” “sports AND LA,” “exercise AND left atrium,” and “exercise AND LA” as the search terms. Eligible studies included those reporting the influence of demographic, anthropometric and athletic characteristics on LA size in athletes. A total of 58 studies were included in this review article. Although LA volume has been reported to be greater in males compared to females when indexed for body surface area (BSA), there was no difference between sexes. The positive association between LA size and age in athletes may reflect the increase in body size with maturation in nonadult athletes and the training age of endurance athletic activity in adult athletes. Caucasian and black athletes have been demonstrated to exhibit similar LA enlargement. The positive association of LA size with lean body mass (LBM) possibly accounts for the relationship of LA size with BSA. LA enlargement has been reported only in endurance‐trained, but not in strength‐trained athletes. LA size appears to increase with an increase in both the volume and intensity of endurance training. LA size correlates independently with the training age of endurance athletes. The athlete's characteristics that independently determine LA size include LBM, endurance training, and training age.

benign in the absence of increased LV filling pressures and mitral valve dysfunction, the excessive LA enlargement in some athletes may challenge the notion of the benign nature of this process. In this respect, the characteristics of the athlete predisposing to LA enlargement are important to be elucidated, since this information will enable the clinician to judge whether the magnitude of LA enlargement in an athlete can be normally expected on the basis of the athlete's characteristics. Furthermore, the importance of the study of characteristics of the athletes with LA enlargement relies on the identification of possible modifiable predisposing characteristics leading to LA enlargement, such as training volume, that, if changed, could decrease the severity of LA enlargement in the case of athletes with atrial arrhythmias. Therefore, this review article discusses the demographic, anthropometric, and athletic characteristics associated with LA enlargement and attempts to elucidate the relative importance of them in determining LA size in athletes. No previous study has addressed these issues.

| Search strategy
A literature search based on PubMed listings up to November 2, 2019 using "athletes AND left atrium," "athletes AND LA," "sports AND left atrium," "sports AND LA," "exercise AND left atrium," and "exercise AND LA" as the search terms identified 3387 articles ( Figure 1). The reference lists of these articles were also interrogated and articles that were judged relevant were selected for inclusion in the review. In total, 58 studies were included in the text of this review article.

| Inclusion criteria
Studies fulfilling the following criteria were considered eligible for inclusion in the review: 1 Original research articles.
2 Studies investigating human individuals.
3 Studies mentioning the influence of demographic, anthropometric or athletic characteristics on LA size in athletes. 4 Full text written in English.

| Gender
The majority of studies have shown that male athletes have greater LA volume compared to female athletes. 7-10 Moreover, George et al demonstrated that among nonadult athletes, LA diameter was increased in males compared to females. 11 Taking into account that LA enlargement usually occurs asymmetrically and LA diameter has been demonstrated to underestimate LA volume especially in females, the comparison of LA size between male and female athletes is more appropriately performed using LA volume rather than LA diameter. 12 However, the difference in LA volume between male and female athletes has been reported to disappear after indexing for body surface area (BSA) or lean body mass (LBM). 9,10,13,14 Considering that females are normally characterized by greater body fat percentage, the persistence in few studies of the difference in LA volume between male and female athletes after indexing for BSA may not represent a valid analysis. 7,15,16 In this case, indexing for the metabolically active LBM is possibly more appropriate. Therefore, the greater LBM of male athletes may account at least in part for their greater LA size.
Nevertheless, the presence of residual confounding cannot be totally excluded in the comparison of LA volume indexed for BSA between male and female athletes, since the training regimens of male athletes are usually characterized by greater volume and intensity, which may in turn affect LA size to a greater extent. Indeed, Mosen et al demonstrated that LA volume indexed for BSA differed only between male and female athletes, but not between male and female controls. 7 Moreover, Legaz Arrese et al reported that LA diameter of long-and middle-distance runners was increased compared to sprint runners; however, this was only F I G U R E 1 Schematic flowchart for the selection of studies to be included in the review The main studies evaluating the effects of demographic, anthropometric and athletic characteristics on left atrial size in athletes

| Age
With regard to the relationship between LA size and age in athletes, LA enlargement has been shown to be more pronounced in adult athletes compared to teenage athletes of the same sport. 18,19 In addition, LA size in athletes has been found to increase with increasing age from childhood to early adulthood. 11,20 However, the relationship between LA size and age from childhood to early adulthood appears to result from the accompanied increase in body size with maturation, rather than from an independent effect of chronological age per se, since the relationship between LA size and age has been found to disappear after adjustment for body size. 19,20 Even more, Somauroo et al showed that among teenage soccer players LA diameter correlated only with BSA and not with age. 21 In the majority of studies, a positive association between LA size and age has been found in adult athletes. 13,15,[22][23][24] Taking into account that this relationship has been shown to be attenuated after adjustment for training age, this association in athletes possibly occurs at least in part through the effect of training age on LA size. 16,25 Indeed, the LA has been reported to progressively enlarge over the years of active athletic life in endurancetrained athletes. 24,26 In other words, the greater number of lifetime endurance training hours of older athletes may determine their greater LA size.
Consistently, LA size in healthy nonathletes has been reported to be determined mostly by body size rather than age and thus an increase in LA size is possibly an expression of pathology and it cannot be attributed to normal aging. 27,28

| Ethnicity
The overwhelming majority of studies evaluating LA size in athletes  Scaling of LA size should be ideally performed for LBM, which is the metabolically active tissue mass in human body. 34 Scaling for body weight, as a proxy measure of LBM, can be precise to the extent that the body fat percentage remains similar across the study population, which is not always the case among athletes of different sports.
Importantly, a common pitfall in allometric scaling of cardiovascular parameters is the inappropriate power to which is raised the allometric parameter used for the scaling of cardiovascular parameters. 34 The ideal scaling procedure should result in body size independent variables. 34 Even more, based on the theory of geometric similarity the one-dimensional LA diameter should be appropriately indexed for LBM 0.3 and BSA 0.5 , while the three-dimensional LA volume for LBM and BSA 1.5 . 11,34,35 Consistently, LA volume indexed for BSA may not be body size independent, as indicated by the reported association between this variable and body mass index in both athletes and nonathletes. 15 Appropriately powered prospective studies are needed to investigate this issue further, such as ascertaining any changes in LA size following weight loss interventions in athletes and nonathletes.
With regard to nonadult athletes, the relationship between LA size and BSA appears to underly the increase in LA size with aging during maturation. 11,20,21,36

| Sport discipline
The degree of LA enlargement in athletes has been found to depend on sport discipline. Specifically, only endurance-trained athletes have been reported to have increased LA size compared to nonathletes, while the LA size of strength-trained athletes has been shown to be similar to age-and gender-matched controls. 16,[37][38][39][40][41][42][43][44][45][46] Of particular interest, there appears to be a more pronounced LA enlargement reported in endurance cyclists. 37,38,40,47 In addition, among athletes performing the same mode of exercise, LA size appears to increase as the endurance component of the sport increases. 17,48 Indeed, LA size was found to be greater in both long-and middle-distance runners compared to sprint runners. 17 Similarly, LA size of baseline tennis players was shown to be increased compared to offensive tennis players, who are known to be characterized by lower energy demands during training and competition compared to the former. 48,49 The effect of endurance training on LA size is possibly mediated through the volume overload of this type of training, resulting in a balanced enlargement of all cardiac cavities. 15,16,42,[50][51][52] Indeed, the ratio of LA volume to LV end-diastolic volume has been shown not to differ among endurance-trained athletes, strength-trained athletes and controls. 42 With regard to sports in which a high body weight confers an advantage to the athlete, such as the position of lineman in American Football, athletes often seek advice for weight gain with the goal of becoming larger than their opponents. These athletes are characterized by greater LA size compared to other type of athletes, while this difference has been found to disappear after indexing for BSA, implying that this difference can be attributed to the greater body size of the former. 53

| Training regimen
Both training volume and intensity appear to determine the effect of endurance exercise training on LA enlargement. The impact of training volume on LA size has been more adequately studied compared to the effect of training intensity. Specifically, among endurance-trained athletes, higher training volumes have been associated with greater LA size. 8,54,55 This pattern was demonstrated to exist even in junior athletes. 56  Importantly, LA size has been shown to increase progressively during the process of a training macrocycle from preseason to end season. [62][63][64][65] However, LA volume in marathon runners has been found not to change following 2 months of detraining from peak prerace performance. 66 Therefore, the evaluation of LA size in athletes should consider the current training status of the athletes with regard to not only the current training regimen, but also the exact phase in the temporal sequence of training periodization.
The increase in LA size during the process of a training macrocycle appears to be associated with a decline in peak reservoir and contraction LA strains after at least 4 months of intensification of exercise training. 32,57,62 The clinical significance of this exercise training-associated decline in LA strain remains to be elucidated. Therefore, further studies are needed using CMR imaging in the evaluation of LA volumes, especially to confirm whether an athlete's characteristic so far considered to have a neutral effect on LA size, such as ethnicity, has indeed no effect.

| Training age
Finally, the incorporation of myocardial mechanical analysis using LA strain can aid in the detection of abnormal LA function even in athletes with normal LA size. 76,77 Importantly, impaired LA strain has been demonstrated to predict not only the development of atrial fibrillation, but atrial fibrillation-related stroke as well, over and above clinical and standard echocardiographic parameters. 78,79 The predictive value of LA strain for the development of atrial fibrillation has also been reported to exist in male endurance veteran athletes. 80 Interestingly, in patients with a normal LA size, LA strain was more predictive of atrial fibrillation, whereas in patients with abnormal LA volumes, LV strain was more predictive of atrial fibrillation. 78 Therefore, it is conceivable that both LA and LV strain (global atrioventricular strain) and associated interrogation of the LA-LV coupling, which provides a comprehensive assessment of left heart mechanics, may contribute to the identification of benign or adverse remodeling that may predispose to the development of atrial fibrillation. In this respect, future studies investigating the impact of athlete's characteristics on LA size should use strain analysis of both LA and LV, in order to elucidate whether the effect of each characteristic on LA size in athletes has any prognostic relevance in terms of predisposition to atrial fibrillation.

| CONCLUSIONS
LA enlargement appears to be a well-established component of the "athlete's heart." The athlete's characteristics that independently determine LA size include LBM, endurance training and training age F I G U R E 2 The direct and indirect effects of demographic, anthropometric and athletic characteristics on left atrial size in athletes. The straight arrows indicate direct effects, while the curved arrows suggest indirect associations ( Figure 2). The effects of gender, age, and ethnicity on LA size in athletes may be mediated through the above-mentioned characteristics.
The accurate interpretation of these variables, which impact LA size in athletes, is of significant clinical importance, in order to ascertain if the LA enlargement detected in an athlete is physiological or represents an underlying cardiac disease.