Association of ECG early repolarization phenomena and “T-infantile” with autonomic regulation of the heart rhythm in young athletes

The incidence of autonomic disorders in athletes varies widely from 6.2 % to 36.5 %. With the improving sport qualification, the frequency and severity of autonomic dysfunction increase. Various ECG phenomena, including SEVR and “T-infantile” are associated with a type of autonomic tone. Moreover, ANS dysfunction does not determine the genesis, but only contributes to the manifestation of these syndromes signs. The association between the ECG phenomena and autonomic dysfunction nature, age and gender of athletes remains an open question.

Scientific works concerning the study of "T-infantile" in children and adolescents are presented both in a cohort of young athletes [6], as well as their peers who are not involved in sports [23,24]. According to M. Gomirato-Sandrucci, G. Bono [17], "T-infantile" is a reflection of the epicardial right ventricular repolarization. "T-infantile" is characterized by inverted and biphasic T-waves in the right precordial leads, while such finding in syndrome of early ventricular repolarization (SEVR) is typical in the left precordial leads and less often in the limb leads. SEVR is associated with the presence of accessory pathway conduction. This phenomenon is a manifestation of atrioventricular conduction abnormalities with functioning of accessory atrioventricular or paranodal pathways.
In this case, a change in the autonomic nervous system tone is important. SEVR occurs when both the parasympathetic and the sympathetic divisions of the autonomic nervous system (ANS) predominate. It is believed that the ANS dysfunction does not determine the genesis, but only contributes to the syndrome signs manifestation. It is thought that SEVR, which is recorded in healthy individuals in the inferior leads in the presence of bradycardia, can serve as a reflection of an increased tone of the parasympathetic nervous system (PNS). However, the shortening of PQ, which is one of the frequent occurrence for SEVR, is not fully consistent with this concept [4].
Attempts to compare the changes in an autonomous homeokinesis found in athletes with the phenomenon of repolarization processes disturbances on the ECG were unsuccessful. According to I. M. Kurbanova, the presence of ST-T-shifts did not statistically significantly increase the frequency of the main symptoms of autonomous dysregulation in young athletes [8].
At the same time, there is convincing evidence that various ECG phenomena are associated with the type of autonomic tone. Signs of increased electrical activity of the left ventricular and right atrial myocardium, as well as lengthening of the electrical systole, are more common for an increased tone of the sympathetic nervous system (SNS). In case of an increased PNS tone, SEVR and pacemaker migration in the atria [8] are relatively more common than in other variants of autonomic tone.
It has been established that in the process of long-term adaptation of the athlete's body, the parasympathetic type of autonomic regulation of the cardiovascular system prevails, physiological hypertrophy of the left ventricle develops, the stroke volume increases, and the myocardial contractility improves. In the process of acute adaptation, adaptive mechanisms are improved, the economization of functions is increased and recovery processes are accelerated [7].
It has been shown that 3/4 of young athletes have autonomic dysfunction with a predominance of cholinergic influences -more often with autonomic overactivity and in-sufficient autonomic provision for activity. Every third athlete is diagnosed with autonomic dysfunction type with increased sympathetic tone associated with more pronounced shifts in the parameters of autonomous homeokinesis. Moreover, with the improving sport qualification, the frequency and severity of autonomic dysfunction increase [8].
The incidence of autonomic disorders in athletes varies widely from 6.2 % to 36.5 %. In the last decade, the prevalence of autonomic disorders has trended upwards in athletes due to an increase in psychophysical stress, environmental condition deterioration, as well as a number of negative social phenomena [9].
The above facts gave occasion to study the relationship between ECG -phenomena "T-infantile" and SEVR and autonomic regulation in young athletes.

Aim
The aim was to study the incidence of juvenile T-wave and SEVR, their association with the heart rate autonomic regulation in young athletes aged between 6 and 17 years.

Materials and research methods
An electrocardiographic study and recording of the heart rate variability using an automated complex "Cardio+" were carried out in 3720 children and adolescents aged between 6 and 17 years, of them 74.6% were boys (n = 2774) and 25.4% were girls (n = 946), engaged in various sports.
In order to assess the state of the neurohumoral regulation mechanisms of the heart, activity of segmental and suprasegmental parts of the ANS, mathematical and spectral methods for analyzing heart rate variability (HRV) were used [10]. In the analysis of HRV, short (5-minute) records were measured in accordance with the International Standard [22].
Analysis of the ANS indices was performed using an integral index of HRV, which was a stress index (SI). According to the recommendation of R. M. Baevsky [2] with SI values less than 50 rel. units, the state was regarded as increased PNS tone, within 51-199 rel. units -as normal ANS tone and the state of increased SNS tone was seen to be at SI above 200 rel. units.
The results were statistically processed using the Statistica for Windows 13 (StatSoft Inc., № JPZ804I382130ARCN10-J) employing parametric methods. The values were given as mean (M) ± standard error of the mean (m). P not exceeding 0.05 was considered as a level of statistically significant differences between indices.
The greatest number of young athletes with juvenile T-wave on the ECG was among boys aged 9-10 years and among 9-, 11-and 12-year-old girls. The most common types of sports practicing by boys and girls were mainly martial arts and sports games, despite the fact that an earlier starting age with sports is currently common for all types of gymnastics (rhythmic, athletic, aesthetic) and diving. The differences in "T-infantile" incidence among young athletes, as compared with the data of other authors, can be attributed to the analysis of different cohorts of athletes involved in other sports, and a number of gender-related factors (hormonal, autonomic, etc.).
The analysis of ECG features in young athletes with the "T-infantile" phenomenon revealed the following.
In girls with "T-infantile" (n = 16), normal sinus rhythm was found in 87.5 % (n = 14) of cases, right atrial rhythm was in 12.5 % (n = 2). Regular rhythm was found in 75 % (n = 12) of athletes and respiratory sinus arrhythmia was in 25 % (n = 4). Normal voltage on ECG was measured in all girls. In 43.75 % (n = 7) of young athletes, the electrical axis of the heart was in semi-vertical position, it was not deviated in 25 % (n = 4) of athletes, its vertical position was in 25 % (n = 4) and right axis deviation was in one (6.25 %) case. Bradycardia was detected in 12.5 % (n = 2), heart rate within 61-79 beats/min -in 50 % (n = 8) and in 37.5 % (n = 6), heart rate was 80 beats/min and more.
In addition to the ECG signs of "T-infantile", incomplete RBBB was seen in three (18.75 %) athletes, and one athlete (6.25 %) showed short PQ syndrome.
A comparative analysis of HRV indices in boys and girls with the "T-infantile" phenomenon found that the D value was significantly higher in boys, reflecting an active vagal control of the heart rhythm regulation (0.403 ± 0.028 s versus 0.311 ± 0.025 s, P = 0.019).

Discussion
The following signs are characteristic for "T-infantile": 1) negative T-wave or a negative phase of two-phased T-wave progressive decrease from lead V1 to lead V4; 2) the apices of negative T-waves or the apices of negative phases of two-phased T-waves in the right precordial leads coinciding or slightly exceeding positive T-waves apices in the left precordial leads; 3) the central depth of T-wave in lead V3 or V4, giving a two-humped shape to it, coincidence with the top of positive T-wave in leads V5, V6; 4) ST segment is on the isoelectric line in the right chest leads without upward convex pattern.
According to N. A. Skuratova [14], signs of "T-infantile" are: 1) negative T-wave apices in the right chest leads coincide (or slightly precede) with positive T-waves in the left chest leads; 2) a reduction in the depth of T-waves negative phase from V1 to V4; 3) the central depth of T-wave coincidence (with two-humped occurrence) in the right precordial leads with the apex of TV5 and TV6 waves; 4) the absence of an arcuate ST segment elevation in the chest leads of the ECG. The described ECG changes in young athletes are a variant of the norm, that have nothing to do with ECG manifestations of cardiomyopathy due to chronic physical stress [1,6].
Elevation of ST segment in combination with negative T-wave in the right chest leads is often detected in black athletes, less often in people with fair skin, and can imitate acute myocardial ischemia. Changes in repolarization in the left chest leads, including ST depression, should be evaluated at different phases of the training cycle, as such changes may be indicative of cardiomyopathy due to physical overstrain in an athlete [18].
In healthy trained athletes, T-waves recorded on an ECG can be high and sharpened, smoothed or isoelectric, prolonged or biphasic as well as inverted. Normally, the amplitude of T-wave changes during physical exercise. With good adaptation to the load, the amplitude of T-wave either remains at the initial level or even slightly increases. If the subject does not tolerate this load, the amplitude of T-wave begins to decrease. Such shifts become larger with a pulse exceeding 150-160 beats/min [13].
The literature data indicate a higher frequency of "T-infantile" registration in healthy children of both sexes aged 7-12 years, with a decrease in the percentage of this ECG phenomenon by 13-17 years. So, according to V. R. Abramova [1], "T-infantile" is registered in 25 % of girls aged 11-12, in 16.6 % of boys aged 11-12 years and in 12.5 % at the age of 13-14 years. M. Gomirato-Sandrucci, G. Bono [17] found "T-infantile" in 30 % of healthy children and adolescents under the age of 14 years, while A. V. Shiyan [16] registered "T-infantile" among 7-9-year-old children in 21.7 %, and among 13-15-year-old in 1.5 %.
Surely, it is not entirely correct to compare the results of our study and the data of A. Pelliccia et al. [21], since Italian researchers combined people under and above the age of 18 years into one group, while the cohort in our study included only children aged 8-17 years. Considering the fact that juvenile T-waves are more common in young people, we made an analogy between the results of these two studies. It should be emphasized that T-wave inversion in more than two precordial and / or standard leads was detected by A. Pelliccia et al. [21] in a slightly higher percentage of persons surveyed than it was in our study (2.3 % versus 1.5 %). The differences in indices are probably due to an age-related heterogeneity and a variation in the sample size.
The frequency of ECG signs combinations detected by A. Pelliccia et al. [21] is also worth mentioning: prolonged PR interval, incomplete RBBB and SEVR. In almost 7% of the examined athletes, mainly (75 %) in young people, these three ECG abnormalities were recorded. We observed a combination of "T-infantile" with incomplete RBBB in 18.75 % of cases in girls and 12.5 % in boys. In addition to this, in boys "T-infantile" was combined with short PQ syndrome in 7.5 % of cases and in 2.5 % -with SEVR.
According to V. I. Pavlova et al., incomplete RBBB is recorded in 50 % of healthy endurance-training athletes. The presence of QRS complex of more than 0.12 seconds or left bundle branch block requires further examination to exclude organic damage to the myocardium [11].
SEVR manifested by an elevation of both J point and ST segment, is observed in 8-9% of athletes. It is necessary to differentiate between SEVR and ECG changes in acute pericarditis [11,18].
Yu. L. Venevtseva and co-authors conducted an ECG examination of 252 students, including 120 Russian-speaking and 13 foreign girls, as well as 54 Russian-speaking and 65 foreign boys. The incidence of SEVR was 5.3 % and 7.7 % in girls, respectively, and 14.8 % and 26.2 % in boys, respectively. HRV was evaluated in all students with a calculation of generally accepted indicators in sitting and standing positions. As a study result, Russian-speaking young men with SEVR showed signs of a relative increase in the parasympathetic influences: on the background of a longer average cardio interval (936.2 ± 42.6 and 809.0 ± 19.3 ms; P = 0.022), they had a lower LF / HF ratio (1.03 ± 0.30 and 2.33 ± 0.35; Р = 0,0047), relative wave power LF% (P = 0.012), AMo%, autonomic equilibrium index (AEI), index of adequacy of regulatory processes (IARP), autonomic rhythm index (ARI) and SI, and higher HF relative wave power (41.1 ± 6.9 and 26.0 ± 1.9 %; P = 0.034), however girls showed only a tendency to such an increase due to a decrease in the LF/HF ratio and the relative power of the vasomotor LF waves in a past history, while there were no differences in orthostasis. SEVR on ECG in foreign young men may indicate an increase in sympathetic influences: the power of high-frequency HF wave in a past history was lower than in boys without this phenomenon (P = 0.048) with a tendency to increase in the LF/HF ratio (P = 0.051). There were no differences in orthostasis [3].
This way, Yu. L. Venevtseva and co-authors received a confirmation of the linkage between an increase in parasympathetic influences and SEVR in Russian-speaking young men. In the study, we also observed the association between increased PNS tone and the ECG-phenomenon "T-infantile" only in young athletes, such a relationship was not observed in girls.
E. V. Pshenichnaya and E. V. Prokhorov examined 547 teenage boys aged 15-16 years, who had come to a clinic to decide on an ability of practicing sport in sports sections, educational institutions with a high level of physical activity. A standard ECG was performed in 311 (56.9 ± 2.1 %) adolescents with identified changes during an objective examination of the cardiovascular system. In 174 (63.0 ± 2.9 %) children, cardiac arrhythmias and conduction disorders were detected: sinus tachycardia in 48 (17.4 ± 2.3 %), sinus bradycardia in 43 (15.6 ± 2.2 %), premature atrial contractions -in 34 (12.3 ± 2.0 %), premature ventricular contractions -in 37 (13.4 ± 2.1 %), atrioventricular block I -in 10 (3.6 ± 1.1 %), the WPW phenomenon -in 2 (0.7 ± 0.5 %). The spectrum of rhythm and conduction disorders and the frequency of their detection according to the standard ECG data did not fundamentally differ from the results of other authors. At the same time, during an additional 24-hour Holter monitoring for all adolescent boys with changes in the standard ECG, heart rhythm disturbances were detected only in 51 (9.3 %) examined [12].
Young athletes with the ECG-phenomenon "T-infantile" can present with cardiomyopathy. According to L. A. Butchenko [5], the following changes were revealed on the ECG in such cases: 1) the absence of a progressive decrease in negative T-wave or a negative phase of two-phased T-wave from lead V1 to lead V4, and even an increase in the negative T-wave or negative phase of the two-phased T-wave towards lead V3; 2) the appearance in one of the leads, more often in the leads V3, V4, of a negative or a positive flat T-wave; 3) final negativization of the T-wave; 4) upward convex pattern of ST-segment elevation. The ECG signs of cardiomyopathy described in young athletes can occur in various combinations.
F. Migliore et al. [19], when examining 2765 children (1914 male and 851 female) between 8 and 18 years old (average age 13.9 ± 2.2 years), recorded T-wave inversion in the right precordial leads in 131 children, which amounted to 4.7 %. The prevalence of "T-infantile" decreased significantly with increasing age (8.4 % of children under 14 years of age compared with 1.7 % of those over 14 years of age, P < 0.001). Of 158 children with T-wave inversion, 4 (2.5 %) were diagnosed with cardiomyopathy, including arrhythmogenic cardiomyopathy of the right ventricle in three and hypertrophic cardiomyopathy in one. The authors suggest that T-wave inversion is a common ECG violation in hereditary heart muscle diseases, such as hypertrophic cardiomyopathy and arrhythmogenic right ventricular cardiomyopathy, which are the main causes of sudden cardiac death in young athletes.
These cardiomyopathies are genetically determined and show age-related phenotypic expression. Since the early manifestations of the disease usually occur after puberty, the persistence of T-wave inversion in post-puberty raises the problem of differential diagnosis between a developing heart muscle disease and a benign juvenile type of repolarization. In this age group, T-wave inversion, localized mainly in the right precordial leads, was documented in 5.7 % of cases, decreased significantly with age, in the puberty, and, most importantly, was a sign of arrhythmogenic right ventricular and hypertrophic cardiomyopathy, verified in 2.5 % of cases. These results showed that following the end of puberty, T-wave inversion is much less common than is widely assumed, and its persistence can indicate a heart muscle disease and a high risk of sudden cardiac death. Therefore, the post-puberty persistence of T-wave inversion in children involved in sports dictates the need for a mandatory echocardiographic examination with the aim of early preclinical verification of heart muscle pathology.
M. Papadakis et al. [20] examined 1710 adolescent athletes and 400 children not practicing sports (control group). The authors did not obtain significant differences in the overall prevalence of T-wave inversion between athletes and the control group (4 % versus 3 %; P = 0.46). T-wave inversion in leads V1-V3 was mainly limited to both groups over the age of 16 years. Only 0.1 % of athletes aged 16 years and older had T-wave inversions beyond V2. T-wave inversion in the inferior and / or lateral leads and deep T-wave inversion occurred infrequently in athletes (1.5 % and 0.8 %, respectively) and were associated with a high prevalence of left ventricular hypertrophy or congenital heart anomalies. Despite an in-depth examination, no athlete was diagnosed with a cardiomyopathy.
Telesheva I. A. and co-authors analyzed 849 ECGs of children aged from 4 months to 17 years who were in a hospital with various somatic diseases in the departments of rheumatology, endocrinology, nephrology, allergology, psychoneurology. Children did not present with complaints concerning cardiological symptoms. During the examination, the authors identified 3 groups of patients in whom the following ECG phenomena were recorded: pacemaker migration (PM), SEVR, supraventricular scallop syndrome (SSS). SSS was most commonly registered, in 40 patients (5 %), PMin 26 (3 %), and SEVR -in 16 (2 %) patients. In none of the cases was a clinically significant cardiological pathology confirmed. The researchers concluded that PM, SEVR and SSS are prognostically and clinically favorable ECG phenomena even in children with concomitant somatic pathology, and do not require further examination and treatment [15].
Thus, SEVR and "T-infantile" are more common in increased PNS tone than in other variants of autonomic tone. A combination of parasympathetic overactivity with these ECG phenomena is observed mainly in males. The phenomenon of "T-infantile" in young athletes of both sexes can be combined with an incomplete RBBB.

Conclusions
1. The prevalence of "T-infantile" among young athletes aged between 6 and 17 years was 1.50 %, 1.07 % in boys and 0.43 % in girls.
2. The highest percentage of young athletes with "T-infantile" was among 9-and 10-year-old boys and among 9-, 11-and 12-year-old girls.
3. In five (12.5 %) athletes, "T-infantile" was combined with incomplete right bundle branch block, in 3 (7.5 %)with short PQ syndrome and in one (2.5 %) -with early repolarization syndrome. 4. The phenomenon of "T-infantile" was combined with incomplete right bundle branch block in three (18.75 %) athletes and with short QT syndrome in one (6.25 %).
5. HRV data indicate the predominance of parasympathetic influences of the autonomic nervous system in boys with the ECG phenomenon "T-infantile", while 50 % of boys and girls with juvenile T-wave have a state of normal ANS tone.
Prospects for further research are to study the effect of exercise on the electrophysiological properties of the myocardium in athletes.