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Table of Contents

    Topic review

    Marathon-Induced Cardiac Fatigue

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    Submitted by: Damien Vitiello

    Definition

    There is a clear impact of marathon on skeletal muscle and myocardium structure. 

    1. Introduction

    The beneficial effect of regular physical exercise on heart function is now widely recognized by researchers in the field of physical activity and sport around the world and more generally in society. Among the main beneficial effects are the improvement of the lipid profile, carbohydrate homeostasis, decrease in resting blood pressure, blood coagulation, improvement of myocardial perfusion and an increase in cardiac output [1]. While the function of the heart pump is improved by regular exercise of moderate intensity [2], it was first shown in 1964 that the function of the left ventricle (LV) was reduced after prolonged physical exercise (PPE) [3]. Almost twenty years later, work has shown impaired cardiac function in athletes who have achieved PPE and used the concept of Exercise-Induced Cardiac Fatigue for the first time [4]. This phenomenon is defined as a transient decrease in systolic and diastolic ventricular functions and is sometimes associated with an increase in markers of myocardial degradation (i.e., cardiac troponins I) [5].

    Endurance activities have been very popular since the end of the 1990′s. The attraction to life in the great outdoors and the desire to know its limits lead more and more people to practice PPE each year [6]. Among these PPE, there are those of moderate duration such as the half-marathon (i.e., between 1–2 h of effort) and the marathon (i.e., 2–4 h), those with long duration such as the semi-triathlon distance “Ironman” (i.e., 5–8 h), and the “Ironman” distance triathlon with its 3.8 km of swimming, 180 km of cycling and 42.195 km of running (i.e., 9–16 h) and those with very long duration such as ultra-marathons or ultra-trails (some events can exceed 24 h). The effect of these PPEs on the cardiac function of participants has been the subject of much scientific research since the end of the 1990′s. The general methodology used in these various works includes the evaluation of echocardiographic parameters of the cardiac function before and after PPE under resting conditions.

    After a marathon running, the majority of studies have reported a decrease in LV and right ventricular (RV) diastolic function. Interestingly, the decrease in diastolic function was effective after 1 h of exercise [7]. More recently, it has been reported that cardiac fatigue is present but with left and right ventricular dysfunction, even more marked than at rest [8]. This study underlined the importance of the intensity of exertion during a marathon in the occurrence of cardiac fatigue. In summary, a moderate duration PPE results in a decrease in LV and RV diastolic function associated with a decrease in ventricular relaxation. The results concerning LV and RV systolic function are contradictory and seem to show that the myocardial alterations are rather dependent on the intensity with which the marathon is performed.

    2. Biomarkers of Cardiac Fatigue and Cardiac Stress after a Marathon

    Sixteen papers were identified in this review and are presented in Table 1. All of them were experimental studies and investigated the change in specific biomarkers between pre- and post-marathon runs. At least 32 different biomarkers were identified in the different studies. The majority of them were biomarker of skeletal muscle and myocardium damage [9][10][11][12][13][14][15][16][17]. In this family, the creatine kinase (CK), the highly sensitive cardiac troponin I and T (hs cTnI; hs cTnT) were mainly measured in the plasma. It was demonstrated that CK and hs cTnT were significantly increased after a marathon run. A second family of biomarkers measured the cardiac injury after marathons [18][11][12][13][15][17][19][20]. The N-terminal pro brain natriuretic peptide (NT-proBNP) was mainly measured in the plasma and was significantly increased after a marathon. In addition, it was reported that the increment of this biomarker immediately after a marathon exhibited a positive curvilinear relationship (r2 = 0.359, p = 0.023) with the running time achieved by the runners [20]. A third family of biomarkers measured the systemic inflammation after marathons [17][21][22]. The interleukin-6 (IL-6) and the tumor necrosis factor-alpha (TNF-alpha) were mainly measured in the plasma. It was demonstrated that both biomarkers were significantly increased after a marathon run.
    Table 1. Cardiac fatigue, cardiac stress and marathon.
    References Methods/Parameters Pre-Marathon Post-Marathon p-Value
      Biomarkers Analyses      
    Traiperm [20]        
      cTnT (ng/mL)      
      NT-proBNP (pg/mL)   Curvilinear relationship between NT-ProBNP increment and running time (r2 = 0.359) <0.05
    Kaleta-Duss [9]        
      CK (U/l) 148 ± 76.3 411 ± 170 <0.001
      hs-cTnI (ng/mL) 0.01 ± 0.01 0.06 ± 0.09 <0.001
      H-FABP (ng/mL) 2.22 ± 1.18 13.57 ± 9.63 <0.001
      BNP (pg/mL) 79.86 ± 53.11 155.38 ± 156.23 <0.001
      NT-proANP (pg/mL) 469.25 ± 155.44 753.3 ± 176.60 <0.001
      Gal-3 (ng/mL) 8.53 ± 3.04 10.65 ± 2.33 <0.001
      GDF-15 (pg/mL) 50.97 ± 27.61 137.34 ± 85.19 <0.001
    Martinez-Navarro [10]        
      hs-cTnT (ng/L) 5.74 ± 5.29 50.4 ± 57.04 <0.001
    Sierra [21]        
      IL-6 (pg/mL) 581 ± 1529 87 ± 53 NS
      IL-8 (pg/mL) 3099 ± 6511 1450 ± 6233 NS
      IL-12p40 (pg/mL) 3775 ± 12406 285 ± 131 <0.05
      IL-23 (pg/mL) 3722 ± 12115 1004 ± 254 <0.05
      IL-33 (pg/mL) 412 ± 1546 267 ± 145 <0.05
      TSLP (pg/mL) 387 ± 1974 20 ± 16 <0.05
      eNO (ppb) 20 ± 11 35 ± 19
    Wegberger [11]        
      Troponin I (µg/L) btw 0–0.01 0.03 (0.02–0.05) 0.016
      CK (U/L) btw 0–250 425 (327–681) 0.001
      Copeptin (pmol/L) btw 0–20 26.25 (16.29–39.02) 0.078
      NT-proBNP (ng/L) btw 0–100 132 (64–198) 0.001
      MR-proADM (nmol/L) btw 0.25–0.60 0.88 (0.55–0.99) 0.023
    de Gonzalo-Calvo [12]        
      hs-cTnT (pg/mL) btw 0–5 btw 0–35 <0.01
      NT-proBNP (pg/mL) btw 0–25 btw 0–110 <0.05
      CK (U/L) btw 0–150 btw 0–300 <0.001
      hFABP (ng/mL) btw 0–3 btw 0–24 <0.01
      Gal-3 (ng/mL) btw 0–7 btw 0–22 <0.001
    Kosowski [13]        
      hs-cTnI (pg/mL) 3.67 (1.88–5.38) 22 (9.58–34.56) <0.001
      NT-proBNP (pg/mL) 50 (33–73) 169 (112–365) <0.001
      ET-1 (pg/mL) 3.03 (2.5–3.4) 5.22 (4.4–5.89) <0.001
      Creatinine (mg/dL) 0.85 (0.79–0.98) 1.39 (1.22–1.56) <0.001
    Richardson [14]        
      cTnT (ng/L) 5.60 ± 3.27 74.52 ± 30.39 <0.001
    Sengupta [18]        
      NT-proBNP (pg/mL) 86.0 ± 9.5 106.5 ± 24.2 0.001
    Clauss [19]        
      Chromogranin A (pg/mL) btw 0–60 btw 0–90 <0.001
      NT-proBNP (ng/mL) btw 0–30 btw 0–110 <0.001
    Roca [15]        
      NT-proBNP (ng/L) 70 (70–70) 92 (70–147) <0.001
      ST2 (ng/mL) 34.2 (24.7–40.9) 54.2 (38.2–72.4) <0.001
      hs-TnT (ng/L) 2.9 (1.7–7) 46.9 (24.1–91.1) <0.001
    Bekos [23]        
      sRAGE (pg/mL) btw 250–600 btw 400–750 <0.001
      ST2 (pg/mL) btw 0–250 btw 125–400 <0.001
    Niemelä [22]        
      suPAR (ng/mL) btw 0.5–2 btw 1.2–3.5 <0.01
      CD163 (ng/mL) btw 300–800 btw 500–1100 <0.05
      CRP (mg/L) btw 0–12 btw 0–22 <0.05
      IL-6 (pg/mL) btw 0–8 btw 17–25 <0.01
      IL-8 (pg/mL) btw 5–12 btw 25–42 <0.05
      IL-10 (pg/mL) btw 0–1 btw 1–3.5 <0.05
      TNF-α (pg/mL) btw 0–1 btw 1–2.5 NS
      TGF-β (pg/mL) btw 500–1000 btw 0–1000 NS
    Martin [16]        
      Creatinine (mg/dL) 0.94 ± 0.12 1.42 ± 0.24 <0.001
      CK (U/L) 133 ± 60 367 ± 167 <0.001
      White blood cells (thousand/μL) 5.75 ± 1.19 15.77 ± 3.29 <0.001
      Neutrophils (cells/μL) 3420 ± 1049 13580 ± 3019 <0.001
    Scherr [17]        
      hs-cTnT (ng/L) 3 (3–5) 31 (19–47) <0.001
      NT-proBNP (ng/L) 27 (14–40) 93 (57–150) <0.001
      h-FABP (Kg/L) 7 (5–10) 45 (32–64) <0.001
      hs-CRP (mg/L) 0.52 (0.30–0.93) 0.40 (0.24–0.85) <0.001
      IL-6 (ng/L) 2.1 (1.9–2.2) 32 (21–41) <0.001
      IL-10 (ng/L) 5.1 (4.9–5.4) 20 (11–50) <0.001
      TNF-α (ng/L) 9 (7–10) 10 (9–12) <0.001
      Cystatin C (mg/L) 0.8 (0.7–0.9) 0.9 (0.9–1.0) <0.001
    Baggish [24]        
      c-miR-1 (fold change)   21.8 0.04
      c-miR-126 (fold change)   1.9 <0.001
      c-miR-133 (fold change)   18.5 0.02
      c-miR-134 (fold change)   1.9 <0.001
      c-miR-146a (fold change)   3.3 <0.001
      hsCRP (fold change)   1.0 1.000
      Echography, HRV & STE analyses      
    Lewicka-Potocka [25]        
      LV EF (%) 61.8 ± 4.9 60.5 ± 4.4 0.38
      LV GLS (%) −19.9 ± 2.3 −19.4 ± 2.1 0.41
      RV 4CSL (%) −22.0 ± 2.8 −20.80 ± 2.6 <0.05
      TAPSE (mm) 25.0 ± 3.6 24.0 ± 3.7 0.56
      RVd MID (cm) 3.4 ± 0.6 3.7 ± 0.5 <0.01
      RVd BAS (cm) 3.8 ± 0.4 3.8 ± 0.5 0.44
      LVd BAS (cm) 4.8 ± 0.4 4.6 ± 0.3 <0.001
      RVd/LVd BAS 0.77 ± 0.1 0.82 ± 0.1 <0.05
    Roeh [26]        
      E/A 1.6 ± 0.5 1.1 ± 0.3 <0.001
      E/e’ mean 6.4 ± 1.5 6.5 ± 1.8 0.6
      DT (s) 0.18 ± 0.05 0.20 ± 0.05 <0.001
      Vmin (mL/m2) 11.4 ± 3.7 9.9 ± 3.5 <0.01
      Vmax (mL/m2) 28.0 ± 6.2 25.0 ± 7.0 <0.01
      Total-SV (mL/m2) 59.6 ± 7.8 60.7 ± 6.0 0.3
      Total-EF (%) 34.9 ± 8.6 31.33 ± 10.2 <0.01
      ASV (mL/m2) 16.6 ± 3.8 15.1 ± 4.1 <0.01
      True-EF (%) 6.1 ± 2.4 4.8 ± 2.8 <0.001
    Sengupta [18]        
      Heart rate (beats/minute) 74.1 ± 6.4 64.5 ± 7.6 <0.001
      Systolic BP (mmHg) 123 ± 11 120 ± 9 0.214
      Diastolic BP (mmHg) 79 ± 5 79 ± 5 0.675
      IVSd (cm) 0.94 ± 0.16 1.03 ± 0.20 0.005
      LV mass (gm) 0.94 ± 0.16 1.03 ± 0.20 0.005
      LV mass (gm) 120.2 ± 30.0 160.3 ± 43.0 <0.001
      LVEDV (mL) 61.8 ± 16.5 72.8 ± 5.1 <0.001
      LVESV (mL) 21.9 ± 7.5 20.3 ± 3.7 0.191
      LVEF (%) 64.9 ± 5.6 72.0 ± 5.7 <0.001
      Mitral E (cm/s) 89.8 ± 17.1 80.1 ± 17.0 0.001
      Mitral annular e0 (cm/s) 10.4 ± 2.1 10.1 ± 2.2 0.638
      Mitral E/e0 9.1 ± 2.4 8.3 ± 2.7 0.227
      Left atrial volume index (mL/m2) 23.2 ± 6.1 19.0 ± 6.5 0.01
      LV global longitudinal strain (%) −19.3 ± 2.71 −16.5 ± 4.6 0.003
      LV global circumferential strain (%) −17.2 ± 2.41 −15.2 ± 2.6 0.001
      LV global radial strain (%) 31.9 ± 7.4 30.9 ± 1.3 0.422
    Mertová [27]        
      Sympathovagal balance - Ln LF/HF
      Heart rate (bpm) - +30  
    Sierra [28]        
      Peak VO2 (mL/kg/min) 51 (46–52) 46 (43–49) <0.05
      Peak VE (L/min) 134 (99–148) 120 (111–147) NS
      VE/VCO2 slope 34 (30–41) 31 (27–39) <0.05
      HR 62 (60–67) 104 (101–111) <0.05
      Systolic volume 80 (79–100) 61 (51–68) <0.05
      Cardiac output 5354(4747–6458) 6234(5238–7433) NS
      LVEDD 51(49–52) 51 (45–58) NS
      LVESD 32 (29–32) 32 (28–34) NS
      EF 67 (66–70) 62 (61–67) NS
      E wave 0.9 (0.7–1.0) 0.6 (0.5–0.7) <0.05
      A wave 0.7 (0.5–0.9) 0.9 (0.8–0.9) NS
      E/A ratio 1.3 (1.1–1.5) 0.7 (0.6–0.8) <0.05
      s’ wave 8.8 (8.2–9.7) 6.7 (5.9–8.0) <0.05
      e’ wave 9.2 (8.4–10.6) 8.5 (6.4–10.4) NS
      a’ wave 8.1 (7.6–9.1) 7.6 (6.6–9.6) NS
      E/e’ ratio 0.09 (0.08–0.10) 0.08 (0.06–0.09) NS
    Hanssen [29]        
      Heart rate (beats/min) 57 ± 7 86 ± 13 <0.001
      Systolic blood pressure (mmHg) 132 ±13 121 ± 12 <0.001
      Diastolic blood pressure (mmHg) 86 ± 8 74 ± 7 <0.001
      LVEF (%) 65 ± 4 67 ± 5 0.280
      LV end-diastolic volume (cm3) 120 ± 25 113 ± 27 0.142
      E (cm/s) 74 ± 14 66 ± 14 0.054
      A (cm/s) 56 ± 13 72 ± 12 <0.001
      E /A ratio 1.4 ± 0.3 0.9 ± 0.2 <0.001
      Septal E’ (cm/s) 10 ± 1 8 ± 2 0.001
      Septal A’ (cm/s) 10 ± 2 12 ± 3 0.001
      E /E’ ratio 8.3 ± 1.6 8.4 ± 3.4 0.871
    Chan-Dewar [30]        
      Sub-epicardial
    radial strain (%)
    32.6 ± 12.5 20.3 ± 9.6% <0.01
      Sub-endocardial circumferential strain (%) −26.9 ± 3.6 −23.7 ± 4.1 <0.01
      EF 63 ± 5 62 ± 7 NS
      E/A 1.8 ± 0.7 1.1 ± 0.2 <0.01
    4CSL: four-chamber longitudinal strain = global strain; ASV: atrial stroke volume; BNP: B-type natriuretic peptide; BP: blood pressure; Bpm: beats per minutes; Btw: between; CK: creatine kinase; DT: deceleration time; E: early diastolic mitral inflow velocity; E/e’: ratio of early diastolic mitral inflow to mitral annular velocity; e’: early diastolic mitral annular velocity; EDD: end-diastolic diameter; EF: ejection fraction; eNo: exhaled nitric oxide; ESD: end-systolic diameter; ESV: end-systolic volume; FAC: fractional area change; Gal-3: galectin 3; GDF-15: growth differentiation factor 15; GLS: global longitudinal strain; H-FABP: heart-type fatty acid binding protein; HRV: heart rate variability; hs-cTnI: high sensitivity cardiac troponin I; IL: interleukin; IVSd: diastolic interventricular septum thickness; LF/HF: low-frequency power/high-frequency power; LV: left ventricle; LVd BAS: LV basal end-diastolic diameter; LVEDD: left ventricular end-diastolic diameter; LVEDV: left ventricular end-diastolic volume; LVEF: left ventricular ejection fraction; LVESD: left ventricular end-systolic diameter; LVESV: left ventricular end-systolic volume; NT-proANP: N-terminal proatrial natriuretic peptide; PWd: posterior wall in diastole; PWs: posterior wall in systole; RV: right ventricle; RVd BAS: RV basal end-diastolic diameter; RVd MID: RV mid-cavity end-diastolic dimension; RVd/LVd BAS: basal RV to LV end-diastolic diameter ratio; S: peak systolic pulmonary venous flow velocity; STE: speckle tracking echography; SV: stroke volume; TAPSE: tricuspid annular plane systolic excursion; Total-EF: total ejection fraction; Total-SV: total stroke volume; True-EF: true ejection fraction. Data are expressed as means, medians and interquartile ranges (25th percentile; 75th percentile) and R-squared.
    4CSL: four-chamber longitudinal strain = global strain; ASV: atrial stroke volume; BNP: B-type natriuretic peptide; BP: blood pressure; Bpm: beats per minutes; Btw: between; CK: creatine kinase; DT: deceleration time; E: early diastolic mitral inflow velocity; E/e’: ratio of early diastolic mitral inflow to mitral annular velocity; e’: early diastolic mitral annular velocity; EDD: end-diastolic diameter; EF: ejection fraction; eNo: exhaled nitric oxide; ESD: end-systolic diameter; ESV: end-systolic volume; FAC: fractional area change; Gal-3: galectin 3; GDF-15: growth differentiation factor 15; GLS: global longitudinal strain; H-FABP: heart-type fatty acid binding protein; HRV: heart rate variability; hs-cTnI: high sensitivity cardiac troponin I; IL: interleukin; IVSd: diastolic interventricular septum thickness; LF/HF: low-frequency power/high-frequency power; LV: left ventricle; LVd BAS: LV basal end-diastolic diameter; LVEDD: left ventricular end-diastolic diameter; LVEDV: left ventricular end-diastolic volume; LVEF: left ventricular ejection fraction; LVESD: left ventricular end-systolic diameter; LVESV: left ventricular end-systolic volume; NT-proANP: N-terminal proatrial natriuretic peptide; PWd: posterior wall in diastole; PWs: posterior wall in systole; RV: right ventricle; RVd BAS: RV basal end-diastolic diameter; RVd MID: RV mid-cavity end-diastolic dimension; RVd/LVd BAS: basal RV to LV end-diastolic diameter ratio; S: peak systolic pulmonary venous flow velocity; STE: speckle tracking echography; SV: stroke volume; TAPSE: tricuspid annular plane systolic excursion; Total-EF: total ejection fraction; Total-SV: total stroke volume; True-EF: true ejection fraction. Data are expressed as means, medians and interquartile ranges (25th percentile; 75th percentile) and R-squared.
    Three of the selected studies measured the heart-type fatty acid binding protein (H-FABP) (i.e., mainly found inside cardiomyocytes) after a marathon [9][12][17]. Despite an important variability between the studies, H-FABP was significantly increased after a marathon run in three studies.
    In addition, two studies measured the galactin-3 (gal-3) which is a protein involved in various biological activities in different organs, including apoptotic regulation, inflammation and fibrosis [9][12]. After a marathon, this protein was significantly increased in both studies. Another two studies measured the suppression of tumorigenicity 2 (ST2) [15][23] after a marathon. They both reported a significant increase of ST2 after running. Technical issues and determination of a diagnostic threshold have to be done to fully recognize the specificity of these biomarkers.
    Finally, only one study investigated the potential of circulating short nonprotein coding RNA (c-miRNA) to explore the impact of a marathon run [24]. In this study, which was conducted with 21 healthy male marathon runners, the authors demonstrated that all plasma levels of the selected c-miRNA (i.e., enriched in muscle: c-miR-1; c-miR-133a; c-miR-499-5p; enriched in myocardium: c-miR-208a; enriched in vascular endothelium: c-miR-126; marker of inflammation: c-miR-146a) were significantly increased when compared to pre-marathon. The authors also stated that these c-miRNAs might represent real-time and tissue-specific adaptation biomarkers of a marathon run.

    3. Cardiovascular Function after Marathon

    Seven papers were identified in this review and are presented in Table 1. All of them were experimental studies and assessed the cardiovascular function before and after a marathon run. The majority of the selected studies used echocardiography alone [18][25][26][28][30]. The majority of these studies reported a decreased E wave and/or an E/A ratio after a marathon. They also all reported no significant difference of the LV EF values between pre- and post-marathon. Three of these studies used the speckle tracking imaging technique to evaluate LV and RV strains [18][25][30]. For LV function, Sengupta et al. reported a significant decrease of the global longitudinal (≈−3% in average) and circumferential (−2% in average) strains but not in the radial plane after a marathon in recreational runners with a mean age of 41 ± 8 years [18]. In their study, Chan-Dewar et al. reported a significant decrease of the LV subepicardial radial strain (−12.3% in average) sub-endocardial circumferential strain (−3.2% in average) in male non-elite marathon runners with a mean age of 32 ± 10 years [30]. On the contrary, Lewika-Potocka et al. did not report any difference for the LV global strain between pre- and post-marathon in amateur marathon runners with a mean age of 40 ± 8 years [25]. However, these authors also analyzed the RV function and they reported a significant decrease of the RV four chambers longitudinal strain after a marathon (−1.2% in average).
    Moreover, one study used the heart rate variability to assess the cardiac autonomous nervous system [27] and one study assessed cardiac function with cardiac magnetic resonance and echocardiography [29], pre- and post-marathon. In the first study, the authors reported a significant increase of the cardiac sympathetic activity (+30 min) and of the heart rate in supine position (+30 bpm) after a skyrunning marathon (i.e., 42 km distance with an ascent distance of 3.15 km and a descent distance of 2.85 km) in healthy male amateurs with a mean age of 37 ± 9 years. In the second study, the authors demonstrated a significant decrease of the LV E/A ratio and of the LV septal E’ and A’ waves after a marathon with male amateur runners with a mean age of 41 ± 5 years. In addition, they demonstrated no difference between pre- and post-marathon for the LV radial shortening and the circumferential and longitudinal strains assessed by MRI. However, the analysis revealed an increase in LV torsion and maximal torsion velocity after a marathon.

    The entry is from 10.3390/ijerph18168676

    References

    1. Nystoriak, M.A.; Bhatnagar, A. Cardiovascular Effects and Benefits of Exercise. Front. Cardiovasc. Med. 2018, 5, 135.
    2. Warburton, D.E.; Nicol, C.W.; Bredin, S.S. Health benefits of physical activity: The evidence. CMAJ 2006, 174, 801–809.
    3. Saltin, B.; Stenberg, J. Circulatory Response to Prolonged Severe Exercise. J. Appl. Physiol. 1964, 19, 833–838.
    4. Douglas, P.S.; O’Toole, M.L.; Hiller, W.D.; Hackney, K.; Reichek, N. Cardiac fatigue after prolonged exercise. Circulation 1987, 76, 1206–1213.
    5. Shave, R.; Baggish, A.; George, K.; Wood, M.; Scharhag, J.; Whyte, G.; Gaze, D.; Thompson, P.D. Exercise-induced cardiac troponin elevation: Evidence, mechanisms, and implications. J. Am. Coll. Cardiol. 2010, 56, 169–176.
    6. Eijsvogels, T.M.; Fernandez, A.B.; Thompson, P.D. Are There Deleterious Cardiac Effects of Acute and Chronic Endurance Exercise? Physiol. Rev. 2016, 96, 99–125.
    7. Middleton, N.; Shave, R.; George, K.; Whyte, G.; Hart, E.; Atkinson, G. Left ventricular function immediately following prolonged exercise: A meta-analysis. Med. Sci. Sports Exerc. 2006, 38, 681–687.
    8. Banks, L.; Sasson, Z.; Busato, M.; Goodman, J.M. Impaired left and right ventricular function following prolonged exercise in young athletes: Influence of exercise intensity and responses to dobutamine stress. J. Appl. Physiol. 2010, 108, 112–119.
    9. Kaleta-Duss, A.M.; Lewicka-Potocka, Z.; Dąbrowska-Kugacka, A.; Raczak, G.; Lewicka, E. Myocardial Injury and Overload among Amateur Marathoners as Indicated by Changes in Concentrations of Cardiovascular Biomarkers. Int. J. Environ. Res. Public Health 2020, 17, 6191.
    10. Martínez-Navarro, I.; Sánchez-Gómez, J.; Sanmiguel, D.; Collado, E.; Hernando, B.; Panizo, N.; Hernando, C. Immediate and 24-h post-marathon cardiac troponin T is associated with relative exercise intensity. Eur. J. Appl. Physiol. 2020, 120, 1723–1731.
    11. Wegberger, C.; Tscharre, M.; Haller, P.M.; Piackova, E.; Vujasin, I.; Gomiscek, A.; Tentzeris, I.; Freynhofer, M.K.; Jäger, B.; Wojta, J.; et al. Impact of ultra-marathon and marathon on biomarkers of myocyte necrosis and cardiac congestion: A prospective observational study. Clin. Res. Cardiol. Off. J. Ger Card Soc. 2020, 109, 1366–1373.
    12. de Gonzalo-Calvo, D.; Dávalos, A.; Fernández-Sanjurjo, M.; Amado-Rodríguez, L.; Díaz-Coto, S.; Tomás-Zapico, C.; Montero, A.; García-González, Á.; Llorente-Cortés, V.; Heras, M.E.; et al. Circulating microRNAs as emerging cardiac biomarkers responsive to acute exercise. Int. J. Cardiol. 2018, 264, 130–136.
    13. Kosowski, M.; Młynarska, K.; Chmura, J.; Kustrzycka-Kratochwil, D.; Sukiennik-Kujawa, M.; Todd, J.A.; Jankowska, E.A.; Banasiak, W.; Reczuch, K.; Ponikowski, P. Cardiovascular stress biomarker assessment of middle-aged non-athlete marathon runners. Eur. J. Prev. Cardiol. 2019, 26, 318–327.
    14. Richardson, A.J.; Leckie, T.; Watkins, E.R.; Fitzpatrick, D.; Galloway, R.; Grimaldi, R.; Baker, P. Post marathon cardiac troponin T is associated with relative exercise intensity. J. Sci. Med. Sport. 2018, 21, 880–884.
    15. Roca, E.; Nescolarde, L.; Lupón, J.; Barallat, J.; Januzzi, J.L.; Liu, P.; Pastor, M.C.; Bayes-Genis, A. The Dynamics of Cardiovascular Biomarkers in non-Elite Marathon Runners. J. Cardiovasc. Transl. Res. 2017, 10, 206–208.
    16. Martin, T.G.; Pata, R.W.; D’Addario, J.; Yuknis, L.; Kingston, R.; Feinn, R. Impact of age on haematological markers pre- and post-marathon running. J. Sports Sci. 2015, 33, 1988–1997.
    17. Scherr, J.; Braun, S.; Schuster, T.; Hartmann, C.; Moehlenkamp, S.; Wolfarth, B.; Pressler, A.; Halle, M. 72-h kinetics of high-sensitive troponin T and inflammatory markers after marathon. Med. Sci. Sports Exerc. 2011, 43, 1819–1827.
    18. Sengupta, S.P.; Mahure, C.; Mungulmare, K.; Grewal, H.K.; Bansal, M. Myocardial fatigue in recreational marathon runners: A speckle-tracking echocardiography study. Indian Heart J. 2018, 70 (Suppl. 3), S229–S234.
    19. Clauss, S.; Scherr, J.; Hanley, A.; Schneider, J.; Klier, I.; Lackermair, K.; Hoster, E.; Vogeser, M.; Nieman, D.C.; Halle, M.; et al. Impact of polyphenols on physiological stress and cardiac burden in marathon runners—Results from a substudy of the BeMaGIC study. Appl. Physiol. Nutr. Metab. Physiol. Appl. Nutr. Metab. 2017, 42, 523–528.
    20. Traiperm, N.; Chaunchaiyakul, R.; Burtscher, M.; Gatterer, H. Cardiac Biomarkers Following Marathon Running: Is Running Time a Factor for Biomarker Change? Int. J. Sports Physiol. Perform. 2021, 1–8.
    21. Sierra, A.P.; Oliveira-Junior, M.C.; Almeida, F.M.; Benetti, M.; Oliveira, R.; Felix, S.N.; Santos Genaro, I. Impairment on Cardiopulmonary Function after Marathon: Role of Exhaled Nitric Oxide. Oxid Med Cell Longev. 2019, 2019, 5134360.
    22. Niemelä, M.; Kangastupa, P.; Niemelä, O.; Bloigu, R.; Juvonen, T. Acute Changes in Inflammatory Biomarker Levels in Recreational Runners Participating in a Marathon or Half-Marathon. Sports Med. Open. 2016, 2, 21.
    23. Bekos, C.; Zimmermann, M.; Unger, L.; Janik, S.; Hacker, P.; Mitterbauer, A.; Koller, M.; Fritz, R.; Gäbler, C.; Kessler, M.; et al. Non-professional marathon running: RAGE axis and ST2 family changes in relation to open-window effect, inflammation and renal function. Sci. Rep. 2016, 6, 32315.
    24. Baggish, A.L.; Park, J.; Min, P.-K.; Isaacs, S.; Parker, B.A.; Thompson, P.D.; Troyanos, C.; D’Hemecourt, P.; Dyer, S.; Thiel, M.; et al. Rapid upregulation and clearance of distinct circulating microRNAs after prolonged aerobic exercise. J. Appl. Physiol. Bethesda Md. 1985. 2014, 116, 522–531.
    25. Lewicka-Potocka, Z.; Dąbrowska-Kugacka, A.; Lewicka, E.; Gałąska, R.; Daniłowicz-Szymanowicz, L.; Faran, A.; Nabiałek-Trojanowska, I.; Kubik, M.; Kaleta-Duss, A.M.; Raczak, G. Right Ventricular Diastolic Dysfunction after Marathon Run. Int. J. Environ. Res. Public Health 2020, 17, 5336.
    26. Roeh, A.; Schuster, T.; Jung, P.; Schneider, J.; Halle, M.; Scherr, J. Two dimensional and real-time three dimensional ultrasound measurements of left ventricular diastolic function after marathon running: Results from a substudy of the BeMaGIC trial. Int. J. Cardiovasc. Imaging 2019, 35, 1861–1869.
    27. Mertova, M.; Botek, M.; Krejci, J.; Mckune, A. Heart rate variability recovery after a skyrunning marathon and correlates of performance. Acta Gymnica 2017, 47, 161–170.
    28. Sierra, A.P.; Silveira, A.D.; Francisco, R.C.; Barretto, R.B.; Sierra, C.A.; Meneghelo, R.S.; Kiss, M.A.; Ghorayeb, N.; Stein, R. Reduction in Post-Marathon Peak Oxygen Consumption: Sign of Cardiac Fatigue in Amateur Runners? Arq. Bras Cardiol. 2016, 106, 92–96.
    29. Hanssen, H.; Keithahn, A.; Hertel, G.; Drexel, V.; Stern, H.; Schuster, T.; Lorang, D.; Beer, A.J.; Schmidt-Trucksäss, A.; Nickel, T.; et al. Magnetic resonance imaging of myocardial injury and ventricular torsion after marathon running. Clin. Sci. Lond Engl. 2011, 120, 143–152.
    30. Chan-Dewar, F.; Oxborough, D.; Shave, R.; Gregson, W.; Whyte, G.; George, K. Left ventricular myocardial strain and strain rates in sub-endocardial and sub-epicardial layers before and after a marathon. Eur. J. Appl. Physiol. 2010, 109, 1191–1196.
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