Cardiology control measurements after returning to high intensity trainings following SARS-CoV-2 infection were performed in 165 asymptomatic elite athletes and 18 symptomatic athletes or athletes with pathological findings.
Results of asymptomatic elite athletes
The analysis was performed in 165 asymptomatic elite athletes (male: 122 (73.9%), age: 20 years (IQR: 17–24 years), training: 16 h/week (IQR: 12–20 h/week)) from various types of sport (Fig. 1), 93.5 days (IQR: 66.8–130.0 days) after the first signs of the infection and after 21 days (IQR: 14–28 days) of training cessation.
Types of sports of the examined asymptomatic elite athletes.
During the acute phase, 28 (17.0%) athletes had asymptomatic infection, 136 (82.4%) had mild symptoms, while 1 (0.6%) athletes had moderate symptoms due to the SARS-CoV-2 infection.
Slightly elevated high-sensitive Troponin T (hs Troponin T) levels were measured in one (0.6%) elite asymptomatic athlete. In this case, slightly elevated hs Troponin T level was present 4 months after the SARS-CoV-2 infection and all other laboratory blood measurements, echocardiography and CPET examinations were negative. After skipping trainings for two weeks, hs Troponin T level normalized according to the control laboratory measurements. Therefore, the hs Troponin change was considered as sports related in this case.
Control echocardiographic examinations proved slightly increased pulmonary pressure in two (1.2%) asymptomatic elite athletes (32 + 5 mmHg and 36 + 3 mmHg), no other supposedly COVID-19-related changes were measured. In these cases, chest x-ray examinations were carried out without any pathological results. Further controls performed 7–14 days later showed normal pulmonary pressure values and no additional abnormalities were recognized. Furthermore, independently from SARS-CoV-2 infection, at the echocardiographic examinations preserved left and right ventricular ejection fraction (n = 1, 0.6%), slight diastolic dysfunction (n = 1, 0.6%), Barlow type mitral valve with mitral annular disjunction (n = 1, 0.6%) and left ventricular hypertrabecularization (n = 2, 1.2%) were revealed.
Most of the asymptomatic elite athletes had satisfactory fitness levels as per the results of CPET. (Table 1.) Resting heart rate was 70 BPM (IQR: 64–79 BPM). During CPET examinations, the athletes achieved a maximum heart rate of 187 BPM (IQR: 181–194.5 BPM) (94.7 ± 4.3% of the calculated maximal heart rate), a maximal relative aerobic power (oxygen uptake, V̇O2max) of 50.9 ± 6.0 ml/kg/min, and a maximal ventilation of 143.7 ± 30.4 l/min. The athletes reached their anaerobic threshold at 87.0 ± 6.4% of their V̇O2max, with a heart rate of 93.2% (IQR: 90.7–95.3%) of their maximal values. The 1-min heart rate recovery was 27 BPM (IQR: 22–34 BPM).
Comparison of CPET results before and after a SARS-CoV-2 infection in elite athletes
In 62 athletes, previous CPET results were also available (Table 1.). Follow-up time between CPET examinations before and after the SARS-CoV-2 infection was 0.74 years (IQR: 0.61–1.78 years). The CPET exercise time proved to be longer after the infection compared to the previous results (pre- vs. post-infection: 13.0 min (IQR: 11.0–15.0 min) vs. 14.0 (IQR: 12.0–15.8) min, p = 0.003). In terms of V̇O2max and ventilation, even higher values were observed on the CPET after the infection compared to the previous examinations. (Fig. 2) The athletes achieved similar maximal blood lactate levels during the exercise tests and spent a similar percentage at the anaerobic phase. At the anaerobic threshold, higher heart rate ratio to the maximal heart rate and similar oxygen uptake ratio to the V̇O2max were measured. (Fig. 3) Compared to the previous results, a slight decrease of maximal heart rate was observed on the CPET after the infection (Table 1.), however, results corrected for age showed no significant change in maximal heart rate (adjusted pre- vs. post-infection: 190.6 ± 12.5 vs. 188.2 ± 12.0 BPM, p = 0.086). No significant differences were observed between VE/CO2 slopes before and after the infection. However, individual cases of decreased exercise capacity (more than 10% decrease of V̇O2max at the post-COVID CPET compared to the previous examinations) were also confirmed by the CPET results (N = 6 [9.7%]).
Maximal oxygen uptake of the examined asymptomatic elite athletes before and after the SARS-CoV-2 infection (n = 62). Abbreviations: VO2, oxygen uptake; *, p < 0.005.
Relative heart rate and oxygen uptake at the anaerobic threshold in relation to the maximal values of the examined asymptomatic elite athletes before and after the SARS-CoV-2 infection. Abbreviations: HR, heart rate; VO2, oxygen uptake; *, p < 0.005.
Detailed evaluation revealed resting or exercise-induced atrial or ventricular arrhythmias or significant ST-T changes (ST-depression, T-wave inversion) in 8 (4.8%) athletes, while no pathological resting or exercise induced corrected QT interval changes (calculated by the Bazett formula) were found in any of the athletes25. In these cases, no direct connection between ECG abnormalities and the infection were proven, but further evaluation and close follow-up were recommended to exclude any potentially malignant arrhythmias or cardiac pathologies. (Table 2.) Behind the above arrhythmias, no structural cardiac abnormalities were revealed by the detailed cardiac evaluation. The exercise induced sustained ventricular tachycardia proved to be a Belhassen-type arrhythmia. Out of the ST-depression cases, one athlete (with descending ST depression and T-wave inversion in inferior leads during the CPET) had non-significant ischemic heart disease, while another one had a coronary artery bridge due to the results of cardiac CT examinations. By hypertensive exercise blood pressure measurements and ambulatory blood pressure monitoring results, new initiation of antihypertensive therapy was necessary in 7 cases. (Table 2).
In 22 (13.3%) asymptomatic elite athletes, just the echocardiography (n = 7, 4.2%) or the CPET examinations (n = 15, 9.1%) revealed cardiovascular pathologies requiring treatment or follow-up. In cases of cardiac pathologies, further examinations, restrictions in sports activity, and follow-up were recommended according to the current European guidelines30.
Results of athletes with positive findings or ongoing symptoms during the second visit
The results of those elite and non-elite athletes who still had symptoms during the second visit or had positive clinical findings (n = 18, elite athlete: n = 9) were evaluated separately and are detailed below.
At the time of the control measurements, 11 athletes were still symptomatic (elite athletes: n = 5), although previously all of them had only mild symptoms in the acute phase of the infection. Symptoms were decreased exercise capacity (n = 4), palpitations (n = 3), exercise-induced shortness of breath (n = 2), worsening symptoms of asthma bronchiale (n = 2), or peripheral skin symptoms (n = 1). (Table 3).
In an asymptomatic case, elevated hs Troponin T levels were measured repeatedly from the first step visit, and similar values were measured during a more than 6-month follow-up. During this time, no symptoms appeared, and all examinations—including cardiac MR—were negative. In this case, the hs Troponin changes were considered as an individual characteristic without cardiac diseases.
One athlete, who previously had mild acute symptoms due to COVID-19 disease for 12 days, suffered from a long-standing mild, stabbing chest pain starting almost 2 weeks after the onset of the first symptoms, and visited our Clinic for the first time 2 months after the starting symptoms of the disease. Due to these late symptoms, a cardiac MR examination was carried out and revealed preserved left and right ventricular ejection fractions, and infero-lateral and apical-lateral sub-epicardial late gadolinium enhancement without oedema as a potential sign of previous myocarditis. A follow-up cardiac MR carried out 8 months later detected the regression of these pathological signs (late gadolinium enhancement area 2020.11.: 9% vs. 2021.07.: 5%). Due to the timing of the infection and in the absence of other infections, this case was considered as a previous COVID-19 myocarditis.
A non-elite master athlete with horizontal ST-depression in V4-V6 precordial leads, proved to have anomalous right coronary artery origin and significant coronary artery disease. The right coronary artery originated from the left aortic sinus of Valsalva and turned immediately rightwards in a very acute angle and traversed in between the pulmonary trunk and the aorta before returning to its normal course (Fig. 4).
The case of a 60-year-old female amateur runner, with non-COVID-19-related findings. In a master female amateur runner with treated hypertension, the SARS-CoV-2 caused mild symptoms, and she still suffered from weakness 3 months after the infection. On her first visit, echocardiography revealed grade I-II. mitral insufficiency and the resting ECG showed incomplete right bundle branch block and horizontal 1 mm ST-depression in V4-V6 leads; no major alterations were found in her laboratory examination. During her second visit, he CPET examination revealed significant horizontal 2 mm ST-depression in V4-V6 (panel A). The patient was referred to cardiac CT, where the right coronary artery had the origin from the left aortic sinus of Valsalva and turned immediately rightwards in a very acute angle and traversed in between pulmonary trunk and aorta before returning to its normal course. Also, on the same artery after leaving the pulmonary trunk and aorta, a significant atherosclerosis was revealed (panel B). Due to these findings, a percutaneous coronary intervention was recommended, which verified the anomalous origin of the right coronary artery and showed the significant stenosis of the same artery (panel C). Therefore, a drug-eluting stent implantation was carried out. Due to the anomalous origin of the right coronary artery, a stress echocardiography was also performed after the intervention to examine cardiac function during exercise. No ischemic regions, or wall motion abnormality was detected. The asymptomatic patient was advised to perform light-to-moderate intensity sport activities.
In an elite athlete, who still had effort dyspnea symptoms at the time of CPET examinations, decreased exercise capacity was observed. This athlete suffered of asthma bronchiale diagnosed before the SARS-CoV-2 infection and treated with optimal medical therapy. However, the symptoms of asthma bronchiale worsened in the long term following the infection. As a consequence, a significant decrease was measured in the fitness status comparing the CPET results before and after the infection. After pulmonary examinations, asthma bronchiale treatment was optimized and the symptoms of the athlete resolved (Fig. 5).
Decreased exercise capacity of a 19-year-old female water polo player after SARS-CoV-2 infection. On the graph, two CPET examinations are shown, between the two exanimations the follow-up time was 0.61 year. The earlier results of the examinations are shown with pale colours, the examinations after the SARS-CoV-2 are shown with sharp lines. The athlete achieved shorter running time on the same CPET protocol, with approximately the same ventilation (brown lines), slightly higher oxygen uptake (blue lines) and carbon dioxide production (red lines), worse metabolic adaptation to sports activity, which is represented by the increased lactate levels (green lines). The aerobic and anaerobic thresholds are represented with two vertical lines during the post-infection examination. In conclusion, multiple negative effects on her fitness status can be observed in this case. Further examinations revealed the worsening of her previously known asthma bronchiale symptoms and her treatment was optimized. Abbreviations: VO2, oxygen uptake; VE, ventilation; VCO2, carbon-dioxide production.
In case of a master athlete, who had palpitations and fatigue after a moderate symptomatic SARS-CoV-2 infection, multiple ventricular premature beats, ventricular couplets, a short non-sustained ventricular tachycardia (5 beats) and multiple supraventricular premature beats were recorded on the CPET. Multiple polymorphic ventricular couplets and a 19-beat-long paroxysmal atrial fibrillation were recorded on the 24-h Holter ECG. Due to the positive findings on the CPET and Holter ECG examinations and to the various cardiovascular risk factors, a cardiac CT was carried out. A borderline significant stenosis was revealed on the proximal part of the right coronary artery. Stress echocardiography was performed for further evaluation, but no ischaemic signs were revealed.
The pathological coronary artery diseases revealed in two amateur master endurance athletes (1 of them asymptomatic with ST-T abnormalities on the resting ECG and 1 with palpitations after SARS-CoV-2 infection) emphasize the importance of cardiology screening and early cardiology evaluation in this higher risk population.
In cases of symptoms or cardiac pathologies, further examinations, restrictions in sports activity, and follow-up were recommended according to the current European guidelines30.
