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ORIGINAL ARTICLE
Division of Cardiology,
Policlinico Casilino, ASL Rome
B, Rome, Italy
2
Department of Health
Sciences, University of Rome
Foro Italico, Rome, Italy
3
The FMSI Sport Medicine
Institute, Villa Stuart Sport
ClinicFIFA Centre of
Excellence, Rome, Italy
4
Department of MedicalSurgical Sciences and
Biotechnologies, University of
Rome La Sapienza, Rome,
Italy
5
Institute of Sports Medicine
and Science (CONI), Rome,
Italy
Correspondence to
Professor Leonardo Cal,
Division of Cardiology,
Policlinico Casilino, ASL
Rome B, Via Casilina 1049,
Rome 00169, Italy;
leonardo.calo@tin.it
Received 1 May 2014
Revised 5 October 2014
Accepted 13 October 2014
ABSTRACT
Objective T wave inversion (TWI) has been associated
with cardiomyopathies. The hypothesis of this study was
that TWI has relevant clinical signicance in peripubertal athletes.
Methods Consecutive male soccer players, aged
818 years, undergoing preparticipation screening
between January 2008 and March 2009 were enrolled.
Medical and family histories were collected; physical
examinations, 12-lead ECGs and transthoracic
echocardiogram (TTE) were performed. TWI was
categorised by ECG lead (anterior (V1V3), extended
anterior (V1V4), inferior (DIIaVF) and infero-lateral
(DIIaVF/V4V6/DI-aVL)) and by age.
Results Overall, 2261 (mean age 12.4 years, 100%
Caucasian) athletes were enrolled. TWI in 2
consecutive ECG leads was found in 136 athletes
(6.0%), mostly in anterior leads (126/136, 92.6%). TWI
in anterior leads was associated with TTE abnormalities
in 6/126 (4.8%) athletes. TWI in extended anterior
(2/136, 1.5%) and inferior (3/136, 2.2%) leads was
never associated with abnormal TTE. TWI in infero-lateral
leads (5/136, 3.7%) was associated with signicant TTE
abnormalities (3/5, 60.0%), including one hypertrophic
cardiomyopathy (HCM) and two LV hypertrophies.
Athletes with normal T waves had TTE abnormalities in
4.4% of cases, including one HCM with deep Q waves
in infero-lateral leads.
Conclusions In this broad population of peri-pubertal
male athletes, TWI in anterior leads was associated with
mild cardiac disease in 4.8% of cases, while TWI in
infero-lateral leads revealed HCM and LV hypertrophy in
60% of cases. ECG identied all cases of HCM.
echocardiographic abnormalities and cardiac symptoms, TWI in anterior leads have traditionally been
considered benign in children.9 Conversely, their
persistence after puberty4 10 11 or their presence in
inferior and lateral leads3 has been associated with
cardiomyopathy.
The hypothesis of this study was that TWI has relevant clinical signicance in peri-pubertal athletes.
Therefore, a systematic application of transthoracic
echocardiogram (TTE) during preparticipation
screening was adopted in a selected population of
peri-pubertal male athletes competing at the regional
level, with or without TWI at ECG.
METHODS
Study population
Consecutive male soccer players undergoing preparticipation screening in the FMSI Sport Medicine
InstituteVilla Stuart Sport Clinic in Rome, Italy,
were enrolled. Eligible athletes had to be never
screened for cardiac disease before. Prior to enrolment, each subject (or the parents of minors) gave
written consent to participate in the study. The
study was approved by the local institutional review
board.
Study procedures
Each participant had a standardised personal and
family medical history review, physical examination
and resting 12-lead ECG and underwent TTE, performed by an expert cardiologist and sport medicine practitioner.
INTRODUCTION
Copyright Article author (or their employer) 2014. Produced by BMJ Publishing Group Ltd (& BCS) under licence.
Special populations
and xed with respiration, marked heart murmurs (any diastolic
or systolic grade >2/6), irregular heart rhythm, and brachial
blood pressure >140/90 mm Hg.4 12 13 Finally, body surface
area (BSA) and body mass index (BMI) were calculated.
ECG
ECGs were performed according to Italian guidelines.8
Recordings were performed at rest using standard 12-lead placement (Mortara, Milwaukee, USA). ECGs were recorded at a paper
speed of 25 mm/s and at a standard gain of 1 mV/cm. Heart rate
and QRS axis were manually calculated. T wave voltages, ST segments, QRS duration, PR interval and QT interval were measured
in each lead with callipers. Two independent sport medicine physicians and a cardiologist retrospectively examined and interpreted
ECG tracings according to European Society of Cardiology (ESC)
recommendations.10 Discrepancies were resolved by consensus.
Each physician was blinded to history and physical examination
data. TWI was diagnosed in the presence of a negative T wave
1 mm in 2 contiguous leads4 and was localised as follows:
anterior leads (V1V3), extended anterior leads (V1V4), inferior
leads (DIIaVF) and infero-lateral leads (DIIaVF/V4V6/IaVL).
TWI in anterior leads was diagnosed in the absence of complete
right bundle branch block.4
ECG diagnosis of LV hypertrophy (LVH) is challenging in
young athletes since the commonly used QRS voltage criteria,
applying to adults,14 lack specicity.15 Therefore, for the electrocardiographic assessment of LVH, both the SokolowLyon
criteria16 and the Romhilt criteria17 were considered. The QT
interval was corrected for heart rate using the Bazett formula.18
ECG abnormalities were divided into common/training-related
(ie, possibly related to physiological athletes heart remodelling)
and uncommon/training-unrelated, in line with ESC recommendations.7 Early repolarisation was dened as J point elevation
manifested either as QRS slurring or notching, ST segment elevation for more than 0.1 mV in at least two contiguous leads.19
Trans-thoracic echocardiography
Bi-dimensional TTEs were performed in left lateral decubitus by
ve different experienced cardiologists, using an Acuson ultrasound device (Siemens Healthcare, Erlangen, Germany). Images
were acquired from parasternal, apical, subcostal and suprasternal windows and were digitally recorded according to the
American Society of Echocardiography guidelines.20 M-mode,
bi-dimensional echocardiographic data, as well as pulsed, continuous and colour Doppler ow mapping were recorded. An
expert cardiologist reviewed each examination retrospectively,
independently and blinded to history; physical examination and
ECG ndings of the athletes. LV internal diameters and wall
thickness measurements were made in M-mode or, alternatively,
by using the leading edge convention.20 Hypertrophic cardiomyopathy (HCM) was dened as a hypertrophied (wall thickness
>12 mm), non-dilated (end-diastolic diameter <45 mm) LV and
one of: impaired diastolic function, enlarged left atrial diameter,
systolic anterior motion of the anterior mitral valve leaet and
associated LV outow tract gradient, asymmetrical pattern of
hypertrophy or family history of HCM.5 21 Valvular heart diseases were evaluated according to European Association of
Echocardiography recommendations.22 23 Quantication of the
RV size was obtained by measuring the mid-cavity and basal trasversal and longitudinal RV diameter in the apical 4-chamber
view.20 RV outow tract was measured from the parasternal short
axis.20 The RV fractional area change and the displacement of
the tricuspid annulus toward the apex in systole were also
2
Statistical analysis
Continuous variables are reported as the meanSD and data
ranges; categorical variables are reported as number and percentage
per category. Continuous variables were analysed with Students t
test and categoric variables with 2 test, when appropriate.
Statistical signicance was considered for p<0.05. Computations
were performed with SPSS V.19 (IBM, Armonk, New York, USA)
and STATAV.11 software (StataCorp LP, Texas, USA).
RESULTS
Study population and clinical findings
Between January 2008 and March 2009, 2261 consecutive male
Caucasian athletes were enrolled. Mean age was 12.4
2.6 years. The demographic and clinical characteristics of the
population, divided in two subgroups, depending on the presence of TWI, are summarised in table 1.
No athlete had known cardiac disease and 26 athletes (1.1%)
were found to have abnormal personal medical history. In all, 42
athletes (1.9%) reported positive family medical history, mostly
for ischaemic heart disease, but also for dilated cardiomyopathy
(one athlete), inter-ventricular septal defect (one case) and aortic
disease (one case). No athletes reported a family history of
sudden cardiac death. A total of 18 athletes (0.8%) had signicant abnormal ndings on physical examination (table 1). In
general, athletes with TWI were younger, with smaller BSA, BMI
and less total training hours. No signicant differences were
found in the family history or physical examination.
Electrocardiographic findings
Electrocardiographic ndings are presented in table 2, in which
ECG abnormalities are categorised by their likely origin:
common/training-related or uncommon/training-unrelated, and
the study population is divided in two subgroups, depending on
the presence of TWI.
The two subgroups were homogeneous for the electrocardiographic parameters, except for heart rate, which was slightly
higher in athletes with TWI, and QRS duration, which conversely, was lower (table 2).
TWI in at least two consecutive leads was found in 136 athletes
(6.0%), distributed in anterior, extended anterior, inferior and
infero-lateral leads in 126/136 (92.6%), 2/136 (1.5%), 3/136
(2.2%) and 5/136 (3.7%) athletes, respectively (table 3).
TWI was more common among individuals aged 810
(75/599, 12.5%) and 1113 years (45/857, 5.2%) than in those
aged 1416 (14/689, 2%) or 1618 years (2/116, 1.8%) (table
3). A signicant association ( p<0.001) was found between age
groups and the distribution of T waves in ECG leads. Other
training-unrelated ECG abnormalities are listed in table 2.
Echocardiographic findings
Echocardiographic ndings in athletes with or without TWI are
presented in table 4. Distribution of various parameters is
depicted in gures 1 and 2.
Athletes with TWI had small ventricular dimensions, walls
thickness and atrial diameter, according to their younger age
(table 4). No differences were found in TTE measurements
indexed by BSA and/or height (table 4). Abnormal TTE was
observed in 9/136 (6.6%) athletes with TWI and in 93/ 2125
(4.5%) athletes without TWI. The distribution of TTE ndings
in athletes, as well as their relationship with TWI localisation in
Cal L, et al. Heart 2014;0:18. doi:10.1136/heartjnl-2014-306110
Special populations
Table 1 Demographic and clinical characteristics of athletes with or without TWI
Characteristics
1
Overall
n=2261
TWI
n=136
p Value
12.42.6 (818)
12.92.3 (818)
113.5 (816)
<0.0001
599 (26.5)
857 (37.9)
689 (30.5)
116 (5.1)
2261 (100.0)
2261 (100.0)
15716 (114196)
5015 (20100)
1.50.3 (0.82.27)
1.60.2 (11.419.6)
11011 (85140)
697 (5090)
7.31.7 (315)
26 (1.1)
8 (0.4)
7 (0.3)
5 (0.2)
4 (0.2)
2 (0.1)
18 (0.8)
14 (0.6)
13 (0.6)
5 (0.2)
5 (0.2)
524 (24.6)
812 (38.2)
675 (31.8)
114 (5.4)
2125 (100.0)
2125 (100.0)
157.714.4 (114196)
5114 (20100)
1.50.3 (0.82.27)
1.580.1 (11.419.6)
109.112.5 (85140)
67.88.9 (5090)
7.41.2 (315)
26 (100)
8 (31)
7 (27)
5 (19)
4 (15)
2 (8)
15 (83)
12 (80)
13 (86)
5 (33)
4 (27)
75 (55.1)
45 (33.1)
14 (10.3)
2 (1.5)
136 (100.0)
136 (100.0)
149.225 (124187)
44.53.5 (2490)
1.350.4 (0.92.13)
1.493.5 (12.418.7)
103.722.3 (85135)
67.512.6 (5085)
71.1 (612)
0 (0)
0 (0)
0 (0)
0 (0)
0 (0)
0 (0)
3 (17)
2 (67)
0 (0)
0 (0)
1 (33)
<0.0001
<0.0001
<0.0001
<0.0001
<0.0001
<0.0001
<0.0001
<0.0001
0.926
0.617
<0.0001
0.184
0.886
DISCUSSION
In this study, we performed comprehensive preparticipation
screening including medical and family history, physical examination, ECG and TTE in 2261 young male soccer players competing at the regional level.
When compared with athletes with normal T waves, those
with TWI had lower total training times, with consequently
higher heart rate values, and were younger, with smaller BSA
and BMI. The two groups were homogeneous for family
history, physical examination, symptoms, electrocardiographic
parameters and indexed echocardiographic measurements. The
prevalence of TWI was 6% in our population and decreased
with age, being exceptional in athletes 14 years. When
present, TWI usually appeared in the V1V3 leads, where it was
rarely associated with cardiac abnormalities. TWI in inferolateral leads was extremely infrequent (ve cases, 0.2% of the
3
Special populations
Table 2 Electrocardiographic findings in athletes with or without TWI
Characteristics
Heart rate (bpm, meanSD)
PR interval (ms, meanSD)
QRS duration (ms, meanSD)
QTc (ms, meanSD)
QRS axis, degrees, meanSD
Common/training-related abnormalities, n (%)
Early repolarisation pattern
Isolated LVH SokolowLyon criteria*
Isolated LVH Romhilt criteria
Sinus bradycardia
Incomplete RBBB
First degree atrio-ventricular block
Uncommon/training-unrelated abnormalities, n (%)
TWI
QRS axis deviation
Left anterior hemiblock
Complete RBBB
Ventricular pre-excitation
Brugada-like early repolarisation
Q wave in infero-lateral leads
Long QT interval
Overall
n=2261
TWI
n=136
p Value
68.712.7 (37110)
13727.1 (80210)
91.110.4 (80150)
39621.0 (307510)
61.2 25.0 (80140)
67.210.2 (37110)
13727 (80210)
91.210.4 (80150)
39621 (307510)
61.225 (80140)
77.23.5 (47102)
1332.4 (80170)
88.810 (80145)
39719 (356440)
5826 (1591)
<0.0001
0.19
0.003
0.46
0.37
853 (37.7)
609 (26.9)
69 (3.1)
534 (23.6)
355 (15.7)
10 (04)
372 (16.4)
219 (9.7)
67 (3.1)
517 (24.3)
287 (12.7)
8 (0.38)
481 (21.3)
390 (17.2)
2 (1.5)
17 (12.5)
68 (3.0)
0 (0)
0.09
0.07
0.19
0.04
0.07
0.34
136 (6.0)
26 (1.1)
9 (0.4)
4 (0.2)
3 (0.1)
2 (0.1)
1 (0.04)
1 (0.04)
0 (0)
25 (1.2)
9 (0.4)
3 (0.14)
2 (0.09)
2 (0.09)
0 (0)
1 (0.05)
136 (100)
1 (0.7)
0 (0)
1 (0.7)
1 (0.7)
0 (0)
1 (0.7)
0 (0)
0.22
0.364
0.44
0.65
0.644
0.735
0.879
V1V3
V1V4
DIIaVF
DIIaVF/V4V6/
DIaVL
810
(N=599)
1113
(N=857)
1416
(N=689)
1718
(N=116)
75 (12.5)
0
0
0
42 (4.9)
1 (0.1)
1 (0.1)
1 (0.1)
8 (1.2)
1 (0.1)
2 (0.3)
3 (0.4)
1 (0.9)
0
0
1 (0.9)
Values are numbers (%). Percentages are calculated from the total number of athletes
in any age group.
Special populations
Table 4 Echocardiographic findings in athletes with or without TWI
Characteristics
Overall
n=2261
TWI
n=136
p Value
End-diastolic diameter, mm
End-diastolic diameter indexed by BSA, mm/m2
End-systolic diameter, mm
End-systolic diameter indexed by BSA, mm/m2
Inter-ventricular septum thickness, mm
Inter-ventricular septal thickness indexed by BSA, mm/m2
Posterior wall thickness, mm
Posterior wall thickness indexed by BSA, mm/m2
RV diameter, mm
RV diameter indexed by BSA, mm/m2
Left atrial diameter, mm
Left atrial diameter indexed by BSA, mm/m2
LV mass, g
LV mass indexed by BSA, g/m2
LV mass indexed by height,2 7 g/h2.7
EF, %
46.35 (2558)
32.24.8 (17.856.2)
27.64.2 (1346)
19.23.3 (732)
7.2 1.3 (414)
51 (313)
7.21.1 (412)
50.9 (2.813)
26.57.6 (1040)
18.45.9 (9.628)
287.8 (1540)
19.56.4 (6.124.4)
107.333.8
72.315 (40260)
32.27 (1389)
68.64.9 (5075)
46.45 (2558)
324.6 (17.856.2)
27.64.2 (1346)
19.13.3 (732)
7.31.2 (411.5)
51 (213)
7.21.1 (511)
50.8 (2.813)
26.57.8 (1040)
18.36 (9.628)
288 (1540)
19.46.5 (6.124.4)
108.333.7
72.315 (40260)
32.37.1 (1389)
68.74.8 (5075)
43.84.5 (3554)
35.55.4 (2252)
25.73.9 (1833.3)
20.83.6 11.230.2)
6.91.4 (514)
5.51.1 (39.5)
6.71.1 (412)
5.40.9 (3.49.5)
253.4 (1837)
20.23.5 (1030)
26.64.1 (1838)
21.54.3 (8.434.4)
91.432
71.315.5 (51200)
326.6 (1662)
695.4 (5075)
<0.0001
0.09
<0.0001
0.08
0.001
0.09
0.08
0.09
<0.0001
0.11
0.001
0.1
<0.0001
0.35
0.09
0.21
Figure 1 Age, heart rate and LV mass distribution in athletes with or without T wave inversion (TWI). Age and HR distribution are depicted at the
top, on the left and on the right, respectively; LV mass and LV mass indexed for height distribution are depicted down, on the left and on the right,
respectively. Whiskers plot highlights differences between groups.
Cal L, et al. Heart 2014;0:18. doi:10.1136/heartjnl-2014-306110
Special populations
Figure 2 End-diastolic and end-systolic diameter, inter-ventricular septum and posterior wall thickness distribution in athletes with or without T
wave inversion (TWI). End-diastolic and end-systolic diameters are depicted at the top, on the left and on the right, respectively; inter-ventricular
septum and posterior wall thickness distribution are depicted down, on the left and on the right, respectively. Whiskers plot highlights differences
between groups.
The aim of our paper was not to identify athletes at risk of
sudden cardiac death through integrated ECG criteria, but to
explore the clinical signicance of TWI itself. Therefore, our
study, like very few others, investigated repolarisation abnormalities in a selected population of pubertal male athletes by systematically performing TTE in all subjects, regardless of TWI
status.
The pubertal phase is challenging because of a potential overlapping between the juvenile pattern and repolarisation abnormalities reecting structural cardiac diseases. In line with
Migliore et al,4 athletes with TWI in our study population were
younger and less trained. However, they had electro and echocardiographic ndings (indexed by BSA) similar to athletes with
normal T waves. The higher heart rate and narrower QRS can
be explained by the lower training time and younger age. In our
population, TWI had a poor ability to identify athletes needing
sport restriction, which varied signicantly with their distribution across ECG leads (table 4, panel A). Indeed, TWI in anterior leads was not associated with cardiomyopathies, including
ARVC, tending to conrm that the benign juvenile pattern
extends up to the age of 14 years. However, this might be
explained also by a low prevalence of ARVC in the Lazio region
where the study was conducted or even by underdiagnosis of
ARVC due to an incomplete phenotype in this young
population.
Consistent with the ndings of Papadakis et al5 and Wilson
et al,26 we observed that the prevalence of TWI in infero-lateral
6
leads was very low and was associated with structural cardiac
abnormalities, including HCM or LVH in three of ve cases; all
three were 13 years old.
LIMITATIONS
The selected subset of athletes enrolled limited the inuence of
sex, ethnicity and age on TWI prevalence and distribution, thus
differentiating our study from the published ones.4 5 However,
any conclusion can be drawn about the clinical signicance of
TWI in athletes of different ages, races and sport disciplines and
female gender. The low prevalence of cardiomyopathies observed
may be related to the young age of athletes, at which the diseases
may not have manifested. A further limitation is represented by
the cross-sectional study design without a clinical, electrocardiographic and echocardiographic follow-up. However, a follow-up
study of this population will be the object of a future publication.
CONCLUSIONS
In our population, TWI in anterior leads was associated with
patent foramen ovale, mitral valve prolapse and bicuspid aortic
valve in 4.8% of cases. Negative T waves in infero-lateral leads
revealed HCM and LVH in 60% of cases. ECG was sufcient to
exclude the two cases of HCM. Implementation of echocardiography allowed us to discover cardiac abnormalities, in some
cases of a serious nature, requiring serial follow-up because of
possible cardiac deterioration over time in athletes with and
without TWI.
Cal L, et al. Heart 2014;0:18. doi:10.1136/heartjnl-2014-306110
Special populations
Figure 3 Relationship between ECG and transthoracic echocardiogram (TTE) ndings in athletes with or without T wave inversion (TWI) at ECG.
Arrows indicate subgroups. PFO, MVP and BAV indicate patent foramen ovale, mitral valve prolapse and bicuspid aortic valve, respectively.
Ethics approval This study has been approved by the local institutional review board.
Key messages
What is already known on this subject?
T wave inversion (TWI) at ECG is relatively rare among athletes
and its clinical signicance is not well known.
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Notes