Cardiac Remodeling in Female Athletes with Relation to Sport Discipline and Exercise Dose – A Cardiac Magnetic Resonance Study

Lukasz A Malek; Barbara Miłosz-Wieczorek; Magdalena Marczak

doi:10.4103/hm.hm_19_22

ORIGINAL ARTICLE

Year : 2022 | Volume : 6 | Issue : 3 | Page : 187-191

Cardiac Remodeling in Female Athletes with Relation to Sport Discipline and Exercise Dose – A Cardiac Magnetic Resonance Study

Lukasz A Malek¹, Barbara Miłosz-Wieczorek², Magdalena Marczak²
¹ Department of Epidemiology, Cardiovascular Disease Prevention and Health Promotion, National Institute of Cardiology, Warsaw, Poland
² Department of Radiology, Magnetic Resonance Unit, National Institute of Cardiology, Warsaw, Poland

Date of Submission	11-Jul-2022
Date of Acceptance	14-Sep-2022
Date of Web Publication	30-Sep-2022

Correspondence Address:
Prof. Lukasz A Malek
Department of Epidemiology, Cardiovascular Disease Prevention and Health Promotion, National Institute of Cardiology, Niemodlinska Str 33, 04-635 Warsaw
Poland

Source of Support: None, Conflict of Interest: None

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DOI: 10.4103/hm.hm_19_22

Abstract

Purpose: To compare chronic cardiac adaptations to exercise at various intensities and in different sports categories of female athletes. Methods: This was a retrospective study including 30 elite female athletes (members of the National Team), 14 amateur female athletes training 3-6 h per week for several years, and 20 inactive female controls who underwent cardiac magnetic resonance. Results: Left and right ventricular end-diastolic volumes (LVEDVI and RVEDVI) differed between all studied groups. They rose from controls to elite athletes, with amateur athletes in-between (for LVEDVI 73 ± 9 vs. 83 ± 6 vs. 95 ± 13 ml/m², P < 0.001, for RVEDVI 74 ± 7 vs. 84 ± 6 vs. 97 ± 14 ml/m², P < 0.001, respectively). Left and right atrial areas (LAA and RAA) were larger in amateur and elite athletes than in controls (P < 0.001), but there was no difference between the two athlete groups. The interventricular septal diameter was mildly higher only in elite female athletes (9 ± 1 mm vs. 8 ± 1 mm, P < 0.001). No difference in the above parameters was found between power and endurance athletes. Three athletes presented with benign myocardial fibrosis in the lower left ventricular (LV)-right ventricle junction point. Conclusions: The hearts of female athletes differed from inactive controls. Part of the changes was related to exercise intensity (LVEDVI and RVEDVI, mild LV muscle thickening), but other changes were not (LAA and RAA). There was no difference in the heart chamber size and LV muscle thickness between studied athletes engaging in power and endurance disciplines. There were also no significant myocardial tissue changes observed in both elite and amateur female athletes.

Keywords: Athlete's heart, endurance, fibrosis, late gadolinium enhancement, power

How to cite this article:
Malek LA, Miłosz-Wieczorek B, Marczak M. Cardiac Remodeling in Female Athletes with Relation to Sport Discipline and Exercise Dose – A Cardiac Magnetic Resonance Study. Heart Mind 2022;6:187-91

How to cite this URL:
Malek LA, Miłosz-Wieczorek B, Marczak M. Cardiac Remodeling in Female Athletes with Relation to Sport Discipline and Exercise Dose – A Cardiac Magnetic Resonance Study. Heart Mind [serial online] 2022 [cited 2023 Mar 29];6:187-91. Available from: http://www.heartmindjournal.org/text.asp?2022/6/3/187/357543

Introduction

Balanced enlargement of the heart chambers (ventricles and atria) with or without mild left ventricular hypertrophy (LVH) is considered a physiological cardiac adaptation to intensive and prolonged physical activity and it is often referred to as an “athlete's heart.”^[1],[2] Most of the data related to this phenomenon come from studies on male athletes, with only a small fraction including females.^[1],[2] The original study in male subjects proposed a different form of adaptation for endurance and power sports with predominant LVH as a result of pressure overload related to Valsalva maneuvers during heavy-weight lifting in power sports and predominant heart chamber dilation mainly without LVH as a result of volume overload in endurance sports.^[3] However, further echocardiographic studies questioned this difference.^{[4],[5],[6],[7],[8],[9],[10]} Little is also known, especially in females, on the relation between the dose of exercise or exercise intensity and the degree of adaptation.

cardiac magnetic resonance (CMR) is nowadays considered a gold standard and free from visualization problems method of assessment of cardiac volumes, mass, and systolic function of the left ventricular (LV) and right ventricle (RV) due to its high spatial resolution and very small intra-and inter-individual variability in judging of the images. This method can also depict the areas of diffused or local myocardial fibrosis typical for irreversible myocardial injury or areas of edema suggestive of myocardial inflammation, which can be used to analyze the risk of intensive exercise to the heart beyond anatomical and functional parameters.^[11]

Therefore, we have decided to use CMR to compare chronic cardiac adaptation to exercise at various intensities (in amateur and elite female athletes) in comparison to inactive women and to assess the differences in cardiac adaptation between elite female athletes engaged in endurance and power sports disciplines.

Methods

Study groups

This was a retrospective study, which included 30 elite female athletes (members of the National Team), 14 amateur female athletes training on average for 3–6 h per week for several years and competing on a local level and 20 inactive female controls. In amateur athletes, the training status was analyzed retrospectively by personal interrogation. Athletes represented endurance (running, rowing, and cycling) and power disciplines (wrestling and judo). The inclusion criteria included the lack of current or prior cardiovascular diseases or cardiovascular symptoms and willingness to undergo cardiac magnetic resonance. Exclusion criteria were: presence of metallic objects in the body or claustrophobia.

Cardiac magnetic resonance

CMR imaging was performed with a Siemens Magnetom Avanto Fit 1.5 Tesla scanner (Siemens, Erlangen, Germany). The protocol included initial scout images, followed by cine steady-state free precession (SSFP) breath-hold sequences in 2-, 3-, and 4-chamber views. The short axis was identified using the 2- and 4-chamber images and included the ventricles from the mitral and tricuspid valvular plane to the apex.

Precontrast T1-mapping and T2-mapping were performed in elite and control subjects right after the acquisition of SSFP cine images using MyoMaps software (Siemens, Erlangen, Germany). For that purpose 3 short-axis slices (one basal, one mid-ventricular, and one apical) were obtained.

This was followed by the administration of 0.1 mmol/kg of a gadolinium contrast agent in all subjects (gadobutrol–Gadovist®, Bayer Pharma AG, Berlin, Germany) flushed with 30 ml of isotonic saline. This was immediately followed by postcontrast vibe sequence acquisition in the axial plane. Late gadolinium enhancement (LGE) images in three long axis and a stack of short-axis imaging planes were obtained with a breath-hold segmented inversion recovery sequence performed 10 min after the contrast injection. The inversion time was adjusted to completely null normal myocardium (typically between 250 and 350 ms). This was followed by postcontrast T1-mapping acquisition 15 min after the contrast injection in the same 3 short-axis slices as the precontrast T1-mapping (in the groups, which underwent native T1-mapping).

Images were analyzed with the use of dedicated scanner vendor software (Syngo. via, Siemens, Erlangen, Germany). Initially, short-axis SSFP cine images were previewed from the base to the apex in a cinematic mode, and then endocardial and epicardial contours for end-diastole and end-systole were manually traced. Delineated contours were used for the quantification of end-diastolic and end-systolic volumes, stroke volumes, ejection fraction, and LV mass, indexed to body surface area (BSA), where necessary. Three-chamber SSFP cine images were used to measure baseline linear dimensions of the left ventricle wall and aorta. Four-chamber cine images were used to obtain the biatrial areas in end-systole. The main pulmonary artery was measured on vibe images. Normal values were based on the published reference.^[12]

All of the maps were of good quality. Precontrast T1 and T2 relaxation times and postcontrast T1 relaxation times were calculated from a 1.5 cm² region of interest (ROI) placed at the mid-ventricular short-axis slice in the mid-section of the interventricular septum. Caution was taken not to include LGE areas in the measurements and not to include blood pool in the ROI. For blood pool pre-and post-contrast T1 time an ROI of the same size was placed at the same level in the ventricular cavity, but separate from the papillary muscles or trabeculations. Extracellular volume (ECV) was calculated using the previously validated equation: ECV = (1-hematocrit) × ([1/T1 myopost-1/T1 myopre]/[1/T1bloodpost-1/T1bloodpre]).^[13] Abnormal native T1 and T2 values were defined as >1054 ms and >50 m, respectively based on previously derived sequence and scanner-specific cutoffs of 2 standard deviations (SDs) above the respective means in a healthy population.^[14] Abnormal ECV values were defined as >32%, which is 2 SDs above the mean observed in our previous study of male athletes.^[15]

Statistical methods

All the results for categorical variables were presented as a number and a percentage. Continuous variables were expressed as mean and SD. Either the Chi-square test or the Fisher exact test was used for the comparison of categorical variables, when appropriate. The Student's t-test for unpaired samples was applied to compare cases and controls. All tests were two-sided with a significance level of P < 0.05. Statistical analyses were performed with MedCalc statistical software 10.0.2.0 (MedCalc, Mariakerke, Belgium).

Ethical considerations

The study had the approval of the Institutional Ethics Committee of the National Institute of Cardiology for the retrospective analysis of data (protocol code IK.NPIA.0021.22.1962/22, date of approval February 10, 2022).

Results

Baseline characteristics and morphological adaptations

All subjects were of similar age, except elite female athletes who were slightly younger than other groups [Table 1]. There was no difference in BSA between the studied groups.

Table 1: Baseline and cardiac magnetic resonance characteristics of the amateur and professional female athletes and inactive female controls

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Left and right ventricular end-diastolic volumes (LVEDVI and RVEDVI) differed between all studied groups. They rose from control subjects to elite athletes, with amateur athletes in-between [for LVEDVI 73 ± 9 vs. 83 ± 6 vs. 95 ± 13 ml/m², P < 0.001, for RVEDVI 74 ± 7 vs. 84 ± 6 vs. 97 ± 14 ml/m², P < 0.001, respectively; [Table 1] and [Figure 1]. LVEDVI and RVEDVI exceeded normal reference values in, respectively, 53% and 47% of elite female athletes and none of the amateur female athletes.

Figure 1: Cardiac magnetic resonance, cine 4-chamber view. Examples of the elite female runner with AH features (a) end-diastole, (b) end-systole and amateur female cyclist without AH features (c) end-diastole, (d) end-systole. (e) small late gadolinium enhancement in the junction point in the elite female athlete (arrow). AH = Athlete's heart

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Left and right atrial areas (LAA and RAA) were larger in both amateur and elite athletes than in control subjects (for LAA 24 ± 4 cm² and 23 ± 4 cm² vs^. 19 ± 4 cm², P < 0.001, for RAA 22 ± 6 cm² and 22 ± 3 cm² vs^. 16 ± 4 cm², P < 0.001), but there was no difference between the two athlete groups [Table 1] and [Figure 1]. LAA and RAA exceeded normal reference values in only 13% and 3% of elite athletes, and LAA was beyond limits in 7% of amateur athletes.

LV muscle thickness represented by interventricular septal diameter and posterior wall diameter (PWd), as well as, total LV mass was higher only in elite female athletes (<0.001 for IVSd and PWd and 0.02 for LVMI) and exceeded normal values in 17%, 3% and 10%, respectively.

No difference between the studied groups was found for left and right ventricular ejection fraction, ascending aorta diameters and pulmonary artery diameter.

Tissue characteristics

LGE representative of myocardial fibrosis was found only in 3 athletes (2 elite and 1 amateur) and in no control subjects. In all cases, it had a form of insertion point fibrosis located in the lower right to LV junction point [Table 1] and [Figure 1]. Parametric imaging (T1-mapping, T2-mapping, and ECV calculation) performed on elite athletes and controls did not reveal any differences suggestive of a lack of edema or diffused fibrosis in both groups.

Endurance versus power sports

Power athletes in the elite group (n = 15, 50%) had higher ECV (28 ± 1 vs. 26 ± 2 cm², P = 0.03) and lower LV ejection fraction (61 ± 2% vs. 63 ± 4%, P = 0.04) than elite endurance athletes (n = 15, 50%). No other differences between those two groups were found.

The main findings of the study are summarized in a graphical abstract [Figure 2].

Figure 2: Graphical abstract summarizing the most important findings in the studied groups of female athletes in comparison to inactive controls

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Discussion

We have demonstrated with means of the CMR that the hearts of female athletes differ from the hearts of their inactive counterparts and that the degree of the observed changes is relative to the intensity of physical activity. It has been previously suggested that the “female athlete's heart” is a less pronounced phenomenon than the “male athlete's heart.”^[1],[2] We have shown that, at least in the elite group, the enlargement of ventricles was also very marked with around 50% of female athletes exceeding reference limits for sex and age. The differences in ventricular volumes, although still visible, were less evident in the amateur female athletes. Interestingly, in female athletes, the atria were less enlarged in comparison to the ventricles, which may explain the lack of increased risk of atrial fibrillation in female athletes.^[16] At the same time, long-term endurance male athletes have a 5–10 times higher risk of atrial fibrillation in comparison to the general population.^[17] We did not observe the difference between atrial size between elite and amateur female athletes. It seems therefore that the ventricular size may be the factor, which better discriminates these two groups in terms of their performance capabilities as in male athletes.^[18] In our study, LV wall thickness was only modestly, although significantly, increased in elite athletes, but not in amateur athletes and reference limits were not offset in most cases. There was also no difference in respect of sports discipline in terms of ventricular size and muscular thickness. It is in line with recent studies questioning the key assumptions of the Morganroth hypothesis or demonstrating data critically verifying this hypothesis in male subjects.^{[4],[5],[6],[7],[8],[9],[10]}

All the findings were possible due to the use of CMR, which is a more accurate imaging method in terms of cardiac volume, mass, and function assessment. Comparative studies between CMR and echocardiography focusing on adaptive changes in athletes showed significant differences between both methods. It turned out that echocardiography overestimates left ventricular mass (LVM) and underestimates LVEDV.^[19] Besides, power sports athletes currently put more attention to endurance training and vice versa. Original Morganroth report may have also included power sport athletes using anabolic steroids which might have led to a marked LV thickness increase not observed in modern times with omnipresent anti-doping testing. The difference in LV ejection fraction and ECV between power and endurance female athletes needs further testing. It is worth noting that both parameters were within reference limits for the normal population.

Importantly, we have not observed any signs of transient (in the form of edema) or irreversible (in the form of fibrosis) myocardial tissue injury. Only three athletes had junction point fibrosis considered benign and therefore clinically insignificant as demonstrated in other studies.^[11],[15] This pattern of LGE was observed earlier in athletes and may be one of the features of the “athlete's heart.” It is believed to arise from increased tension between the left and RV in periods of volume and pressure overload of the heart during intensive exercise.^[11],[15]

Our study has some limitations. First of all, due to a retrospective nature, we were not able to demonstrate the course of cardiac adaptation to exercise. Therefore, the observed differences between female athletes and controls and concerning the intensity of physical activity might have been attributed not only to training but also to congenital causes thus favouring top sports performance in the studied elite athletes or willingness to exercise in the amateur athletes. Secondly, we were not able to analyze the tissue characteristics in the group of amateur athletes. However, the lack of pathologies and no differences in myocardial tissue characteristics between elite female athletes and controls can be probably extrapolated to amateur female athletes.

Conclusions

The hearts of female athletes differ from inactive controls. Part of the changes is related to exercise intensity (more pronounced left and right ventricular enlargement, mild LV muscle thickening in elite athletes), but other changes are not (an increase in LAA and RAA). There is no difference in the heart chamber size and LV muscle thickness between studied athletes engaging in power and endurance disciplines. Importantly, there is also no transient (edema) or irreversible (fibrosis) changes observed in both elite and amateur female athletes.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

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