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Heart Online First, published on November 7, 2014 as 10.1136/heartjnl-2014-306110
Special populations
ORIGINAL ARTICLE
Echocardiographic findings in 2261 peri-pubertal
athletes with or without inverted T waves at
electrocardiogram
Leonardo Calò,1 Fabio Sperandii,1,2 Annamaria Martino,1 Emanuele Guerra,1,2
Elena Cavarretta,3,4 Federico Quaranta,2† Ermenegildo de Ruvo,1 Luigi Sciarra,1
Attilio Parisi,2 Antonia Nigro,3 Antonio Spataro,5 Fabio Pigozzi2
▸ Additional material is
published online only. To view
please visit the journal online
(http://dx.doi.org/10.1136/
heartjnl-2014-306110).
1
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
Clinic—FIFA 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 Calò,
Division of Cardiology,
Policlinico Casilino, ASL
Rome B, Via Casilina 1049,
Rome 00169, Italy;
[email protected]
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 significance in peripubertal athletes.
Methods Consecutive male soccer players, aged
8–18 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 (V1–V3), extended
anterior (V1–V4), inferior (DII–aVF) and infero-lateral
(DII–aVF/V4–V6/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 significant 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 identified 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 significance 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
Institute—Villa 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.
Medical history and physical examination
INTRODUCTION
To cite: Calò L, Sperandii F,
Martino A, et al. Heart
Published Online First:
[please include Day Month
Year] doi:10.1136/heartjnl2014-306110
The prevalence and clinical significance of T wave
inversion (TWI) at ECG in young athletes has been
a subject of investigation.1–5 Previous studies have
shown that TWI in leads V1–V2 are relatively rare
among athletes, with a prevalence ranging from
2.5%, to 4.7%,4 and 0.8% when they extend to
V3.5 TWI in infero-lateral leads has been described
in 1.5%–1.8% of postpubertal Caucasian athletes,5 6
and inverted T waves confined to lateral leads were
observed in 0.1%–0.3% of young athletes.4 5
Although independent from training-related physiological cardiac remodelling,7 8 in the absence of
Personal medical history was considered positive in
case of exertional chest pain or discomfort,
syncope or near-syncope during or after exercise,
palpitations, and in the presence of shortness of
breath or fatigue out of proportion.4 12 13 Family
medical history was considered positive when close
relatives had experienced a premature (<40 years)
heart attack or sudden death, or had cardiomyopathies, Marfan syndrome, channelopathies, severe
arrhythmias, or other disabling cardiovascular diseases.4 12 13 Positive physical findings included
musculoskeletal and/or ocular features suggestive of
Marfan syndrome, diminished and/or delayed
femoral artery pulses, mid- or end-systolic clicks, a
second heart sound that was single or widely split
Calò L, et al. Heart 2014;0:1–8. doi:10.1136/heartjnl-2014-306110
1
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Special populations
and fixed 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 (V1–V3), extended anterior leads (V1–V4), inferior
leads (DII–aVF) and infero-lateral leads (DII–aVF/V4–V6/I–aVL).
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 specificity.15 Therefore, for the electrocardiographic assessment of LVH, both the Sokolow–Lyon
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 athlete’s heart remodelling)
and uncommon/training-unrelated, in line with ESC recommendations.7 Early repolarisation was defined 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
five 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 flow mapping were recorded. An
expert cardiologist reviewed each examination retrospectively,
independently and blinded to history; physical examination and
ECG findings 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 defined 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 leaflet and
associated LV outflow 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 Quantification 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 outflow 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
calculated.20 Arrhythmogenic RV cardiomyopathy (ARVC) was
diagnosed in accordance to current guidelines.11
Statistical analysis
Continuous variables are reported as the mean±SD and data
ranges; categorical variables are reported as number and percentage
per category. Continuous variables were analysed with Student’s t
test and categoric variables with χ2 test, when appropriate.
Statistical significance 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 significant abnormal findings on physical examination (table 1). In
general, athletes with TWI were younger, with smaller BSA, BMI
and less total training hours. No significant differences were
found in the family history or physical examination.
Electrocardiographic findings
Electrocardiographic findings 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 8–10
(75/599, 12.5%) and 11–13 years (45/857, 5.2%) than in those
aged 14–16 (14/689, 2%) or 16–18 years (2/116, 1.8%) (table
3). A significant 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 findings in athletes with or without TWI are
presented in table 4. Distribution of various parameters is
depicted in figures 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 findings
in athletes, as well as their relationship with TWI localisation in
Calò L, et al. Heart 2014;0:1–8. doi:10.1136/heartjnl-2014-306110
Downloaded from http://heart.bmj.com/ on November 8, 2014 - Published by group.bmj.com
Special populations
Table 1 Demographic and clinical characteristics of athletes with or without TWI
Characteristics
1
Age, years, mean±SD
Age groups, n (%)
8–10 years
11–13 years
14–16 years
17–18 years
Male gender, n (%)
Caucasian ethnicity, n (%)
Height, cm, mean±SD
Weight, kg, mean±SD
Body surface area, m2, mean±SD
Body mass index, mean±SD
Systolic blood pressure, mm Hg, mean±SD
Diastolic blood pressure, mm Hg, mean±SD
Total training time, h/week, mean±SD
Medical history abnormalities, n (%)†
Presyncope
Syncope
Palpitations
Exertional chest pain
Excessive exertional dyspnoea and fatigue
Physical examination abnormalities, n (%)‡
Heart murmurs ≥2/6
Split second heart sound
Mid- or end-systolic clicks
Others§
Overall
n=2261
Normal T waves n=2125
TWI
n=136
p Value
12.4±2.6 (8–18)
12.9±2.3 (8–18)
11±3.5 (8–16)
<0.0001
599 (26.5)
857 (37.9)
689 (30.5)
116 (5.1)
2261 (100.0)
2261 (100.0)
157±16 (114–196)
50±15 (20–100)
1.5±0.3 (0.8–2.27)
1.6±0.2 (11.4–19.6)
110±11 (85–140)
69±7 (50–90)
7.3±1.7 (3–15)
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)
157.7±14.4 (114–196)
51±14 (20–100)
1.5±0.3 (0.8–2.27)
1.58±0.1 (11.4–19.6)
109.1±12.5 (85–140)
67.8±8.9 (50–90)
7.4±1.2 (3–15)
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)
149.2±25 (124–187)
44.5±3.5 (24–90)
1.35±0.4 (0.9–2.13)
1.49±3.5 (12.4–18.7)
103.7±22.3 (85–135)
67.5±12.6 (50–85)
7±1.1 (6–12)
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
–
–
–
–
Data ranges are presented in parentheses.
†The sum of subpercentages is not equal to 1.1 because of approximations.
‡More than one abnormality could be present in the same patient.
§Includes fourth sound (two cases), pectus excavatum (two cases) and reinforced second sound (one case).
TWI, T wave inversion.
ECG leads, is depicted in figure 3. There were no cases of
ARVC. Only 6 out 126 (4.8%) athletes with TWI in the anterior leads had minor TTE abnormalities, including patent
foramen ovale (three cases: one age 8, two age 10), mitral valve
prolapse (two cases: one age 10, one age 12) and bicuspid
aortic valve (one age 12). No athletes with TWI in the extended
anterior or inferior leads had any echocardiographic findings.
Among the five subjects with infero-lateral TWI, 3 (60.0%) had
significant TTE abnormalities, including one HCM (a
13-year-old) and two LVH (one age 16, one age 17); the
remaining two had normal TTEs.
The vast majority of athletes without TWI (2032/2125,
95.6%) had normal TTE findings. However, cardiac abnormalities, in some cases serious, were found in 93 children (4.4%),
including: HCM (one), mild LVH (six), mild LV dilation (LVD)
(six), inter-atrial septal defect (13), bicuspid aortic valve (16),
patent foramen ovale (24), inter-atrial septal aneurysm (14),
mitral valve prolapse (eight), patent ductus arteriosus (two), and
pulmonary artery dilation or subvalvular pulmonic membrane
(two and one, respectively). In the athlete with HCM and
normal T waves, ECG revealed deep Q waves in infero-lateral
leads, suggestive of cardiomyopathy.
Sensitivity, specificity, positive and negative predictive
values of TWI for preparticipation screening
The sensitivity and specificity of TWI in identifying cardiac TTE
abnormalities mandating sport restriction (ESC guidelines for
Calò L, et al. Heart 2014;0:1–8. doi:10.1136/heartjnl-2014-306110
preparticipation screening12) were 0.7% (95% CI 0.004% to
0.0012%) and 100% (95% CI 0.997% to 1.000%), respectively.
The positive and negative predictive values were 50% (95% CI
0.479% to 0.521%) and 94.0% (95% CI 0.929% to 0.949%),
respectively. The sensitivity, specificity and predictive values of
TWI according to their localisation on the surface ECG, in
detecting TTE abnormalities needing clinical follow-up and in
identifying cardiac electro-structural abnormalities mandating
sport restriction12 or needing clinical follow-up are presented in
the online supplementary appendix (table S1A, B respectively).
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 V1–V3 leads, where it was
rarely associated with cardiac abnormalities. TWI in inferolateral leads was extremely infrequent (five cases, 0.2% of the
3
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Special populations
Table 2 Electrocardiographic findings in athletes with or without TWI
Characteristics
Heart rate (bpm, mean±SD)
PR interval (ms, mean±SD)
QRS duration (ms, mean±SD)
QTc (ms, mean±SD)
QRS axis, degrees, mean±SD
Common/training-related abnormalities, n (%)
Early repolarisation pattern
Isolated LVH Sokolow–Lyon 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
Normal T waves n=2125
TWI
n=136
p Value
68.7±12.7 (37–110)
137±27.1 (80–210)
91.1±10.4 (80–150)
396±21.0 (307–510)
61.2 ±25.0 (−80–140)
67.2±10.2 (37–110)
137±27 (80–210)
91.2±10.4 (80–150)
396±21 (307–510)
61.2±25 (−80–140)
77.2±3.5 (47–102)
133±2.4 (80–170)
88.8±10 (80–145)
397±19 (356–440)
58±26 (−15–91)
<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
Data ranges are presented in parentheses.
*Sokolow–Lyon criteria:16 RV1+SV5 >35 mm.
†Romhilt criteria:17 RV2+SV5-V6 > 40 mm.
‡Left (≤–30°) or right (≥+120°) axis deviation.
LVH, LV hypertrophy; QTc, corrected QT interval; RBBB, right bundle branch block; TWI, T wave inversion.
study population) and was associated with HCM or LVH in a
high percentage of cases (3/5, 60.0%). Echocardiographic
abnormalities were present in 4.4% (93/2125) of athletes with
normal ventricular repolarisation, including one HCM and a
number of other conditions potentially related to chronic
cardiac disease requiring serial follow-up. The sensitivity of
TWI in identifying cardiac structural abnormalities mandating
sport restriction was 0.7%, while the specificity was 100%, with
positive and negative predictive values of 50% and 94.0%,
respectively.
When TWI is present in competitive athletes, ruling out cardiomyopathies is mandatory. The prevalence and distribution of
TWI are influenced by age and ethnicity. In fact, the prevalence
Table 3 Athletes with negative T waves by age group and ECG
lead localisation
Age groups (years)
V1–V3
V1–V4
DII–aVF
DII–aVF/V4–V6/
DI–aVL
8–10
(N=599)
11–13
(N=857)
14–16
(N=689)
17–18
(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.
4
of TWI ranges from 0.43% in young, Caucasian athletes24 to
39% in adolescent African/Afro-Caribbean ones.25
TWI is rare in postpubertal athletes, in whom it may be associated with cardiomyopathy. In a cohort of 1005 athletes aged 24
±6 years (75% men),2 only 27 athletes had TWI. In a heterogeneous population of 1220 athletes aged 22.6±6 years, TWI in
anterior and lateral leads was absent in Caucasian subjects, in
whom no cardiomyopathies were observed.26 In another study27
involving 510 athletes aged 19±0.3 years, only three subjects
with TWI were identified; interestingly, one was diagnosed with
HCM.
The prevalence of TWI is less infrequent among postpubertal
athletes, where it may be associated with cardiomyopathies.
Marek et al reported a 0.43% prevalence of Twave abnormalities
in a population of 32 561 high school students (51% boys).24 In
their cohort of 32 652 amateur athletes (median age 17 years),
Pelliccia et al28 reported 2.3% of TWI in precordial leads.
Sharma et al29 observed TWI in 4% of 1000 junior elite athletes
aged 15.7±1.4 years. Meanwhile, Di Paolo et al25 compared a
different population of 154 adolescent African soccer players
aged 15.9±0.7 years with 62 Caucasian players, revealing that
TWI was largely present in adolescent Africans and never associated with cardiac disease. Noteworthy, Papadakis et al5
observed a 4% prevalence of TWI among 1710 (age 16
±1.7 years) well trained, postpubertal athletes of various ethnicities.5 TWI beyond right precordial leads was observed in only
0.1% of athletes and was never associated with cardiomyopathies.5 TWI in the inferior or lateral leads was rare, and associated with LVH, mitral valve prolapse or atrial septal defects.5
While the prevalence of TWI in postpubertal athletes has
been intensively investigated, few studies have explored the
Calò L, et al. Heart 2014;0:1–8. doi:10.1136/heartjnl-2014-306110
Downloaded from http://heart.bmj.com/ on November 8, 2014 - Published by group.bmj.com
Special populations
Table 4 Echocardiographic findings in athletes with or without TWI
Characteristics
Overall
n=2261
Normal T waves n=2125
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, %
46.3±5 (25–58)
32.2±4.8 (17.8–56.2)
27.6±4.2 (13–46)
19.2±3.3 (7–32)
7.2 ±1.3 (4–14)
5±1 (3–13)
7.2±1.1 (4–12)
5±0.9 (2.8–13)
26.5±7.6 (10–40)
18.4±5.9 (9.6–28)
28±7.8 (15–40)
19.5±6.4 (6.1–24.4)
107.3±33.8
72.3±15 (40–260)
32.2±7 (13–89)
68.6±4.9 (50–75)
46.4±5 (25–58)
32±4.6 (17.8–56.2)
27.6±4.2 (13–46)
19.1±3.3 (7–32)
7.3±1.2 (4–11.5)
5±1 (2–13)
7.2±1.1 (5–11)
5±0.8 (2.8–13)
26.5±7.8 (10–40)
18.3±6 (9.6–28)
28±8 (15–40)
19.4±6.5 (6.1–24.4)
108.3±33.7
72.3±15 (40–260)
32.3±7.1 (13–89)
68.7±4.8 (50–75)
43.8±4.5 (35–54)
35.5±5.4 (22–52)
25.7±3.9 (18–33.3)
20.8±3.6 11.2–30.2)
6.9±1.4 (5–14)
5.5±1.1 (3–9.5)
6.7±1.1 (4–12)
5.4±0.9 (3.4–9.5)
25±3.4 (18–37)
20.2±3.5 (10–30)
26.6±4.1 (18–38)
21.5±4.3 (8.4–34.4)
91.4±32
71.3±15.5 (51–200)
32±6.6 (16–62)
69±5.4 (50–75)
<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
Data ranges are presented in parentheses.
BSA, body surface area by Moesteller formula; TWI, T wave inversion.
prevalence and significance of TWI among younger athletes. In
particular, Migliore et al4 observed negative T wave prevalence
of 4.7%, 0.9% and 0.1% in the right precordial, inferior, and
lateral leads, respectively, in a population of athletes aged 13.9
±2.2 years. A 2.5% prevalence of cardiomyopathies (three
ARVC and one HCM) was present among athletes with TWI.
However, the prevalence of cardiac abnormalities among individuals without TWI was not assessed.
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.
Calò L, et al. Heart 2014;0:1–8. doi:10.1136/heartjnl-2014-306110
5
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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 significance 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 reflecting 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 findings (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 significantly with their distribution across ECG leads (table 4, panel A). Indeed, TWI in anterior leads was not associated with cardiomyopathies, including
ARVC, tending to confirm 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 findings 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 five cases; all
three were ≥13 years old.
LIMITATIONS
The selected subset of athletes enrolled limited the influence 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 significance 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 sufficient 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.
Calò L, et al. Heart 2014;0:1–8. doi:10.1136/heartjnl-2014-306110
Downloaded from http://heart.bmj.com/ on November 8, 2014 - Published by group.bmj.com
Special populations
Figure 3 Relationship between ECG and transthoracic echocardiogram (TTE) findings 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 significance is not well known.
Provenance and peer review Not commissioned; externally peer reviewed.
Data sharing statement The authors declare that the data of the research article
are original.
REFERENCES
1
What might this study add?
This study reported a poor association of cardiac structural
abnormalities (assessed through systematic transthoracic
echocardiography) with TWI in anterior and inferior leads at ECG in
a broad population of peri-pubertal Caucasian male soccer players.
This study also observed that TWI in infero-lateral leads was
associated with transthoracic echocardiogram (TTE) abnormalities in
60% of cases, including one case of hypertrophic cardiomyopathy
and two cases of LV hypertrophy. TTE abnormalities, including one
case of hypertrophic cardiomyopathy, have been described in 4.4%
of athletes with completely normal T waves.
How might this impact on clinical practice?
In peri-pubertal Caucasian male soccer players, TWI in anterior leads
is benign, while negative T waves in infero-lateral leads raise suspicion
of structural cardiac abnormalities, particularly in older boys.
Acknowledgements We would like to thank Dr Luigi de Matteis for his assistance
during the composition of the paper.
Contributors LC conceived and designed the paper. FS, AM, EG and EC
performed the analysis and interpretation of data and participated in the preparation
of the manuscript. QF, EdR, LS, AP, AN, AS and FP performed the interpretation of
the data and participated in the preparation of the manuscript. All the authors have
read and approved the paper.
Competing interests None.
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Calò L, et al. Heart 2014;0:1–8. doi:10.1136/heartjnl-2014-306110
Downloaded from http://heart.bmj.com/ on November 8, 2014 - Published by group.bmj.com
Echocardiographic findings in 2261
peri-pubertal athletes with or without inverted
T waves at electrocardiogram
Leonardo Calò, Fabio Sperandii, Annamaria Martino, Emanuele Guerra,
Elena Cavarretta, Federico Quaranta, Ermenegildo de Ruvo, Luigi
Sciarra, Attilio Parisi, Antonia Nigro, Antonio Spataro and Fabio Pigozzi
Heart published online November 7, 2014
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