From the Interuniversity Cardiology Institute of the Netherlands, Utrecht
(B.M.P., H.W.M.K., A. vd L., A. d R., E.E. vd W.), and the Departments of
Cardiology (B.M.P., F.L., H.P.B., A. vd L., H.W.V., E.E. vd W.), Radiology
(H.J.L., H.W.M.K., A. d R.), and Medical Statistics (A.H.Z.), Leiden
University Medical Center, The Netherlands.
Correspondence to Ernst E. van der Wall, MD, PhD, Department of Cardiology, Building 1, C5-P25, Leiden University Medical Center, Albinusdreef 2, 2333 ZA Leiden, The Netherlands. E-mail vanderwall{at}cardio.azl.nl
Methods and Results—We studied 21 elite cyclists and 12 healthy
control subjects. Left ventricular mass, volume, and
function were determined by cine MRI. Myocardial high-energy phosphates
were examined by 31P magnetic resonance spectroscopy. There
were no significant differences between cyclists and control subjects
for left ventricular ejection fraction (59±5% versus
61±4%), left ventricular cardiac index (3.4±0.4 versus
3.4±0.4 L · min-1 · m-2), peak
early filling rate (562±93 versus 535±81 mL/s), peak atrial filling
rate (315±93 versus 333±65 mL/s), ratio of early and atrial filling
volumes (3.0±1.0 versus 2.6±0.6), mean acceleration gradient of early
filling (5.2±1.4 versus 5.8±1.9 L/s2), mean deceleration
gradient of early filling(-3.1±0.9 versus -3.2±0.7
L/s2), mean acceleration gradient of atrial filling
(3.6±1.8 versus 4.5±1.7 L/s2), and atrial filling
fraction (0.23±0.06 versus 0.26±0.04, respectively). Cyclists and
control subjects showed similar decreases in the ratio of myocardial
phosphocreatine to ATP measured with 31P magnetic resonance
spectroscopy during atropine-dobutamine stress (1.41±0.20
versus 1.41±0.18 at rest to 1.21±0.20 versus 1.16±0.13 during
stress, both P=NS).
Conclusions—Left ventricular hypertrophy
in cyclists is not associated with significant abnormalities of cardiac
function or metabolism as assessed by MRI and spectroscopy.
These observations suggest that training-induced left
ventricular hypertrophy in cyclists is
predominantly a physiological phenomenon.
Magnetic Resonance Imaging
Flow-Velocity Measurements
Magnetic Resonance Image Analysis
Flow-Velocity Measurements
31P Magnetic Resonance Spectroscopy
Atropine-Dobutamine Infusion Protocol
Statistical Analysis
Both groups had similar blood pressures under resting conditions. Only
resting heart rate was significantly lower in cyclists than in control
subjects (52±6 versus 61±4 bpm, P<.0001).
LV Anatomy and Function
Flow Velocity Measurements
Hemodynamic Data
Metabolic Data
Intraobserver and Interobserver Variability in Mitral Flow
Measurements
The main observation of the present study was the demonstration
that highly trained cyclists with LV hypertrophy have
normal LV systolic and diastolic properties. In
addition, we found a similar decrease in myocardial PCr/ATP ratio
during high workloads caused by atropine-dobutamine stress
in cyclists and sedentary control subjects. This study extends our
previous findings in cyclists,17 in whom we
demonstrated a normal systolic function and normal cardiac
metabolism at rest. The present findings therefore
support the concept that LV hypertrophy in cyclists is a
physiological adaptation without significant
adverse effects on cardiac function and metabolism.
Physiological Versus Pathological LV
Hypertrophy
Diastolic Function
However, interpretation of these measurements can be difficult, because
they are influenced not only by changes in the intrinsic LV
diastolic properties but also by factors such as age, heart
rate, body mass index, blood pressure, valvular disease,
loading conditions, and contractility of both
ventricular and atrial
myocardium.41 Conclusions about LV
diastolic function should therefore be made only after
correction for these parameters.
In our study, the differences in blood pressure or body mass index
between the two groups of subjects were negligible. The cyclists had a
significantly lower resting heart rate and were slightly younger than
the control subjects, although this difference in age did not reach
statistical significance.
With advancing age, the relative contribution of early
diastolic filling diminishes, whereas the atrial filling
becomes more prominent, resulting in a decreased ratio of early to
atrial filling.42 43 With increasing heart rate,
the diastolic filling pattern changes in favor of atrial
contribution, together with a decrease of the velocity area of the
early diastolic filling time and a decrease of the
deceleration time, resulting in a lower ratio of the early to late peak
filling rates and a lower ratio of early to late filling
volumes.44 45 46
Our study found a significantly higher ratio of peak early to atrial
filling volumes in cyclists compared with control subjects,
corresponding to slightly altered LV diastolic properties
in cyclists. However, after correction for age and heart rate, the
cyclists demonstrated a normal diastolic filling pattern,
with no significant differences in parameters such as peak
early filling rate, peak atrial filling rate, early filling volume,
atrial filling volume, ratio of early to atrial filling volumes, mean
acceleration gradient of early filling, mean deceleration gradient of
early filling, mean acceleration gradient of atrial filling, and atrial
filling fraction. Also, there was no significant difference in LV
ejection fraction between cyclists and control subjects. These data
indicate that LV hypertrophy in cyclists is not associated
with significant changes in systolic or diastolic
LV function. We could not confirm the findings of Nishimura at
al,9 who found significantly depressed resting
systolic LV function in 40- to 49-year-old cyclists, or the
findings of Miki et al,10 who demonstrated a
decreased ratio of early to atrial filling velocities in 40- to
60-year-old cyclists. Our findings are, however, in agreement with
other previous Doppler echocardiographic studies in
cylists47 48 49 50 and other
athletes43 49 51 52 53 54 55 56 57 58 that demonstrated normal or
enhanced LV function parameters. To the best of our
knowledge, our study is the first to use MRI in the assessment of LV
systolic and diastolic function in the athlete's
heart.
Myocardial Metabolism With Increased Work
State
Compared with control subjects, the cyclists of the present study
showed a similar decrease in myocardial PCr/ATP ratio in response to a
more than threefold increment in rate-pressure product caused by
atropine-dobutamine infusion. This finding argues against a
greater vulnerability to myocardial ischemia in the athlete's
heart than in control hearts under stress conditions. This lack of
evidence for stress-induced ischemia in the athlete's heart is
particularly noteworthy because the cyclists achieved an even higher
rate-pressure product than the control subjects. A decline in
myocardial PCr/ATP ratio with a threefold increment in rate-pressure
product has not been observed previously in normal human
hearts.65 66 The increase in rate-pressure
product from rest to stress was 1.3 in the study of Conway et
al66 and was not fully described by Kuno et
al.65 The results obtained in our control group
are consistent with previous experimental studies regarding
myocardial responses to increased stress induced by
dobutamine infusion.63 67 68 This
consistency provides further evidence that the
metabolic changes observed in the present study are
more closely related to work state than to LV
hypertrophy.70
Potential Limitations
A relative drawback of spectroscopy is the relatively large voxel size
required for an adequate signal (60x70x70
mm3). Although we carefully avoided inclusion of
skeletal muscle, diaphragm, or liver tissue, we could not completely
avoid contamination of the voxel by contribution of blood. Blood
correction was performed, because blood contains only ATP and no PCr,
which may therefore alter the observed PCr/ATP
ratio.69 However, voxels obtained from
hypertrophied hearts are expected to be less contaminated with blood
because of increased myocardial wall thickness in the athletes.
Last, we can of course not fully exclude the presence of
coronary artery disease in our population, with a mean age of
42 years in the cyclists and a mean age of 47 years in the control
subjects. However, because of complete absence of any cardiac
complaints at rest and during exercise and the lack of major
coronary risk factors, the estimated prevalence of
coronary artery disease is
Conclusions
Received June 26, 1997;
revision received October 9, 1997;
accepted October 27, 1997.
© 1998 American Heart Association, Inc.
Clinical Investigation and Reports
Functional and Metabolic Evaluation of the Athlete's Heart By Magnetic Resonance Imaging and Dobutamine Stress Magnetic Resonance Spectroscopy
Abstract
Top
Abstract
Introduction
Methods
Results
Discussion
References
Background—The question of whether
training-induced left ventricular hypertrophy
in athletes is a physiological rather than a
pathophysiological phenomenon remains unresolved.
The purpose of the present study was to detect any abnormalities in
cardiac function in hypertrophic hearts of elite cyclists and to
examine the response of myocardial high-energy phosphate
metabolism to high workloads induced by
atropine-dobutamine stress.
Key Words: hypertrophy • magnetic resonance imaging • metabolism • spectroscopy • stress
Introduction
Top
Abstract
Introduction
Methods
Results
Discussion
References
Athlete's heart is
the term used for training-induced left ventricular (LV)
hypertrophy in athletes.1 2 3 The
question of whether the enlarged heart of athletes is a purely
physiological phenomenon or should be considered a
risk factor comparable to pathological LV hypertrophy
induced by hypertension or hypertrophic
cardiomyopathy is still
unresolved.4 5 6 Concern has been raised by the
reports of sudden deaths occurring in athletes, possibly related to LV
hypertrophy.7 8
Echocardiographic studies have demonstrated reduced
diastolic properties in several older elite cyclists,
suggesting that in the long run, extreme physical training may have a
negative effect on the heart, manifested by partly irreversible LV
hypertrophy and impaired LV
filling.9 10 Previous studies of the
morphological and functional aspects of the athlete's heart used
echocardiography.2 11 12 13 In
recent years, magnetic resonance techniques with the capability of
assessing cardiac mass, function, and metabolism
(31P magnetic resonance spectroscopy) became
available.14 15 16 A recent study from our
institution demonstrated normal systolic function
parameters and a normal high-energy phosphate
metabolism in elite cyclists at
rest.17 In that study, however, we did not
investigate diastolic function or high-energy phosphate
metabolism during stress. Because abnormalities of
diastolic filling may precede abnormalities of
systolic function in the early stages of disease, we considered
it important to evaluate diastolic function in cyclists as
well.18 In addition, we acquired
31P magnetic resonance spectra at rest and during
atropine-dobutamine stress conditions. The aim of the
present study was (1) to detect the presence of abnormalities in
systolic and diastolic function at rest in the
hypertrophic hearts of elite cyclists and (2) to investigate the
response of myocardial high-energy phosphate metabolism in
these hearts to high workloads induced by
atropine-dobutamine stress. To this purpose, we used MRI
and 31P magnetic resonance spectroscopy.
Methods
Top
Abstract
Introduction
Methods
Results
Discussion
References
Study Population
The study group consisted of 21 male elite cyclists (mean age,
42±8 years; range, 28 to 52 years) and 12 male healthy volunteers
(mean age, 47±8 years; range, 33 to 56 years) matched for height and
weight. The athletes cycled 
12 000 km/y; their duration of athletic
history was 23±7 years (range, 13 to 35 years). The 12 control
subjects were healthy individuals, none of whom were engaged in
sporting activities other than recreation. All individuals were free of
known cardiovascular disease and were normal by
physical examination. They were all nonsmoking, normotensive, and had a
negative family history of coronary heart disease. A standard
12-lead ECG was recorded at rest, which was normal in the control
subjects. In 14 cyclists (67%), the resting ECG met the Sokolow-Lyon
voltage criteria of LV hypertrophy (sum of amplitudes of S
wave in V1 and R wave in V5
or V6 >3.5 mV). The study was approved by the
Human Research Committee at our institution, and all individuals gave
informed consent.
Anatomic and Functional Assessment
MRI was performed with a Philips Gyroscan ACS-NT system (Philips
Medical Systems) operating at 1.5 T and ECG gating. Magnetic resonance
images were acquired with breath-hold multishot echo-planar imaging as
described previously.19
Volume flow was assessed with magnetic resonance velocity
mapping of flow across the mitral orifice and through the
aorta.20 Velocity maps were acquired with a flip
angle of 30°, an echo time of 10 to 12 ms, a section thickness of
8 mm, a field of view of 350 mm, and two measurements of a
128x128 pixel acquisition matrix. The number of time frames varied
according to heart rate, resulting in a temporal resolution of 25 to 30
ms. The maximum phase shift of 180° was set to occur with a velocity
of 100 cm/s for mitral flow and 150 cm/s for aortic flow. Velocity
aliasing was not encountered. To acquire data during late
diastole, velocity mapping was performed with retrospective
gating. Data were collected continuously during the cardiac cycle.
Retrospectively, each measurement was attributed to the point in time
of the cardiac cycle it represented, with the
simultaneously recorded ECG used as a reference. From
the recorded data, a series of velocity maps was reconstructed that
represented an average cardiac cycle during the acquisition
interval.
Anatomic and Functional Assessment
Multislice, multiphase, short-axis image analysis was
performed with the MR analytical software system
MASS21 and a SUN IPX workstation (Sun
Microsystems Computer Corp). End-diastolic and
end-systolic epicardial and endocardial contours of the stack
of short-axis image sections were traced manually. Papillary muscles
were outlined and included in the LV wall. LV mass and LV ejection
fraction were calculated as described previously by our
institution.22
Volume flow was calculated by tracing a region of interest along
the borders of the mitral valve and the borders of the aorta in all
time frames of a velocity map series. For each time frame,
instantaneous volume flow was calculated by a computer algorithm by
multiplying spatial average flow velocity and the area of the region of
interest. Summation of all instantaneous volume flow data yielded total
flow per cardiac cycle. All measurements were performed twice by one
observer on two separate occasions at least 2 weeks apart and once by a
second observer. The following parameters of
diastolic function were measured or derived (Fig 1
): LV stroke volume (mL), peak early
filling rate (mL/s), early filling volume (mL), peak atrial filling
rate (mL/s), atrial filling volume (mL), ratio of peak early and peak
atrial filling rates, ratio of early and atrial filling volumes, mean
acceleration gradient of early filling (
,
L/s2), mean deceleration gradient of early
filling (ß, L/s2), mean acceleration gradient
of atrial filling (
, L/s2), and atrial filling
fraction.
View larger version (30K):
[in a new window]
Figure 1. A, Normal transmitral filling pattern in a
cyclist. Stroke volume is total area under curve (mL); peak early
filling rate is maximal flow rate of first peak (mL/s); early filling
volume equals area under first peak (mL); early filling time is
duration of first peak (ms); atrial filling rate is maximal flow rate
of second peak (mL/s); atrial filling volume equals area under second
peak (mL); atrial filling time is duration of second peak (ms); and
atrial filling fraction is flow volume during atrial filling (area
under second peak) divided by stroke volume (total area under curve).
B, Schematic transmitral filling pattern in a cyclist. Mean
acceleration of early filling is indicated by ; mean deceleration of
early filling by ß; and mean acceleration of atrial contraction by
.
Highly reproducible 31P magnetic resonance
spectra of the anterior wall of the left ventricle were acquired at
rest and during atropine-dobutamine stress in 18 cyclists
and 11 control subjects.23 A 1.5-T Gyroscan S15
(Philips Medical Systems) was used, with a 10-minute,
three-dimensional, image-selected in vivo spectroscopy protocol as
described previously.19 31P
magnetic resonance spectra were transferred to a remote SUN-SPARC
workstation to be quantified automatically by model function
analysis in the time domain, with a priori spectroscopic
knowledge used to improve the accuracy of the spectral
parameters.24 The ATP level in the
spectra was corrected for the relative contribution of ATP present
in the blood.25 Signal modeling, prior knowledge,
and correction for partial saturation effects were applied as in a
previous study.23
After the baseline spectrum was recorded, 0.03 mg/kg
atropine sulfate was administered in three separate doses of 0.01 mg/kg
to achieve complete cholinergic blockade.26
Thereafter, myocardial stress was induced by administration of
incremental intravenous doses of dobutamine,
which increases myocardial oxygen consumption by positive inotropic and
chronotropic effects on the heart. Dobutamine infusion was
started at a dose of 10 µg · kg-1
· min-1 and was increased every 2 minutes at 5
µg · kg-1 ·
min-1 until a steady target heart rate was
reached. The maximum allowed infusion rate was 40 µg ·
kg-1 · min-1. The
target heart rate (bpm) was 85% of the predicted maximal heart
rate.27 Blood pressure was recorded
automatically every 2 minutes at rest and every minute during
dobutamine stress with a Dinamap sphygmomanometer
(Criticon). Dobutamine infusion was discontinued
prematurely if one of the following criteria for termination was met:
chest discomfort, serious arrhythmias, noncardiac side effects
such as nausea and anxiety, systolic blood pressure >220
mm Hg, and diastolic blood pressure >110 mm Hg. In
the present study, no such events occurred.
Data are expressed as mean values±SD. Intraobserver and
interobserver variabilities for the stroke volume, derived from the
mitral flow measurements, were expressed as mean percent error, which
equals the average of differences in flow measurements between
observers divided by average values of the observations, multiplied by
100. Differences between cyclists and control subjects were tested by
Student's t test, and adjustments for age and heart rate
differences between cyclists and control subjects were made by ANCOVA.
A value of P<.05 was considered to be statistically
significant.
Results
Top
Abstract
Introduction
Methods
Results
Discussion
References
Subject Characteristics
The anthropometric characteristics of the 21 cyclists and 12
control subjects are presented in Table 1. Athletes and control subjects were
similar with regard to anthropometric parameters such as
age, height, body mass, and body surface area.
View this table:
[in a new window]
Table 1. Subject Characteristics
LV anatomic and functional parameters of the 21
cyclists and 12 control subjects are presented in Table 2. Cyclists had a 45% increase in LV
mass compared with control subjects (P<.001). In addition,
indexed LV mass, absolute and indexed LV end-diastolic
volume, and ratio of LV mass to volume were also significantly
increased in cyclists compared with control subjects (all
P<.001). Also, LV stroke index was significantly larger in
cyclists than in control subjects (65±7 versus 56±6
mL/m2, P<.005), but because of the
significantly lower heart rate of the cyclists, this did not result in
a significantly increased cardiac index under resting conditions. There
was no significant difference in LV ejection fraction between the two
groups (59±5 in cyclists versus 61±4% in control subjects).
View this table:
[in a new window]
Table 2. Left Ventricular Anatomic
and Functional Parameters
LV diastolic function parameters are
presented in Table 3 and Fig 1
.
There were no significant differences between cyclists and control
subjects in peak early filling rate, peak atrial filling rate, early
filling volume, atrial filling volume, ratio of early to atrial filling
volumes, mean acceleration and mean deceleration gradients of early
filling, mean acceleration gradient of atrial filling, and atrial
filling fraction. The peak ratio of the early to atrial filling rates
was significantly higher in athletes than in control subjects (1.9±0.5
versus 1.6±0.2, P=.043), but after correction for age and
heart rate, this difference was no longer significant
(P=.23).
View this table:
[in a new window]
Table 3. Flow Velocity Measurements
The responses of the hemodynamic variables to
the administration of atropine-dobutamine are shown in
Table 4. Significant increases in heart
rate, blood pressure, and rate-pressure product were observed in
cyclists and control subjects (all P<.001). There was no
significant difference in rate-pressure product at rest between the
two groups. However, during stress, the rate-pressure product of
the cyclists was significantly higher than that of control subjects
(25.9±2.4x103 versus
23.3±3.0x103 mm Hg/min,
P=.016).
View this table:
[in a new window]
Table 4. Hemodynamic and
Metabolic Data in 18 Cyclists and 11 Control Subjects
During Atropine-Dobutamine Stress
The myocardial phosphocreatine (PCr)/ATP ratio decreased
significantly during atropine-dobutamine stress in athletes
and in control subjects (Table 4). In cyclists, the PCr/ATP ratio
decreased from 1.41±0.20 to 1.21±0.20 (P<.001); in
control subjects, the PCr/ATP ratio diminished from 1.41±0.18 to
1.16±0.13 (P<.001). The decrease, however, was similar in
both groups (0.20±0.21 versus 0.24±0.15, P=NS). Examples
of in vivo 31P magnetic resonance spectra
acquired at rest and during atropine-dobutamine stress in a
cyclist and a healthy volunteer are shown in Fig 2.
View larger version (17K):
[in a new window]
Figure 2. Representative cardiac
31P magnetic resonance spectroscopy spectra of a cyclist
and a control subject at rest and during
atropine-dobutamine stress. , ß, and
represent the -, ß-, and -ATP peaks, respectively. DPG
indicates 2,3-diphosphoglycerate; Pi, inorganic phosphate; and PCr,
phosphocreatine.
Intraobserver variability for the mitral flow measurements,
representing LV stroke volume, was 4.8%. The interobserver
variability was slightly higher (5.9%).
Discussion
Top
Abstract
Introduction
Methods
Results
Discussion
References
The primary aims of our study were to assess systolic and
diastolic function at rest in the hypertrophic hearts of
highly trained cyclists and to investigate the response of myocardial
high-energy phosphate metabolism during pharmacological
stress. To this purpose, we used MRI, velocity mapping, and
31P magnetic resonance spectroscopy.
Intense long-term physical training is well known to cause
LV hypertrophy.2 Endurance cycling
ranks among the type of sports with the highest impact on LV
mass.28 In the present study, a substantial
increase in LV mass was found in cyclists compared with control
subjects (45%), which is in agreement with previous magnetic resonance
and echocardiographic studies on athlete's
heart.11 29 30 31 Whether the athlete's heart
carries an increased risk for cardiovascular events
remains an intriguing clinical problem, because LV
hypertrophy in the general population has been shown to be
an independent risk factor for cardiovascular morbidity
and sudden cardiac death.6 An early
characteristic of LV hypertrophy resulting from disease
states such as hypertension,32 33 34 hypertrophic
cardiomyopathy,35 and other
hypertrophic conditions36 is a change in
diastolic properties. Diastolic dysfunction can
therefore serve as a sensitive and early indicator of disease and may
be used to differentiate between physiological and
pathological hypertrophy.37 In
addition, profound changes in cardiac metabolism may
discriminate between physiological and pathological
hypertrophy.
LV diastolic function is commonly assessed by
study of the pattern of ventricular filling through the
mitral valve. Doppler echocardiography is
generally regarded as the noninvasive technique of choice for the
assessment of ventricular filling because of its clinical
utility, wide availability, and low cost. Cine magnetic resonance
velocity mapping is a relatively new method that may add important
information to Doppler echocardiographic data,
because flow is obtained three-dimensionally.38
It therefore makes possible the calculation of both average velocity
and flow in the great arteries and across cardiac valves. This method
has been validated previously at our
institution.20 39 Manifestations of abnormal
diastolic relaxation are, among other things, a diminished
extent and rate of LV filling in early diastole, an
increased contribution of atrial contraction to diastolic
filling, and a decreased ratio of flow in the early rapid filling phase
to that in the atrial contraction phase.40
31P magnetic resonance spectroscopy can be
used to study myocardial metabolism noninvasively by
measuring the relative proportions of high-energy
phosphates.59 Abnormalities of high-energy
phosphate metabolism have been described in studies of
failing hypertrophied human hearts60 61 and in
animal hearts with severe LV
hypertrophy.62 However, imbalances in
energy production and utilization in less severely
hypertrophied hearts may become apparent only under stress conditions.
In addition, existing abnormalities have been observed to become
manifest during stress, with larger changes in hypertrophied than in
normal hearts.59 62 63 64
Exercise-induced cardiac stress is the most
physiological and, therefore, most desirable form
of stress. However, spectral acquisition during exercise-induced
cardiac stress is subject to several limitations, such as motion
artifacts due to movements and increased respiration of the patient and
the low level of exercise presently
attainable.66 Pharmacological stress appears to
be the most suitable alternative for conventional exercise, because it
is characterized by absence of motion artifacts induced by patient
motion and excessive ventilation during exercise. 
5.5% in both groups of
subjects.71
LV hypertrophy in cyclists is not associated with
significant abnormalities of systolic or diastolic
function. During dobutamine-atropine stress, the PCr/ATP
ratio determined in the LV myocardium of cyclists
decreased, but this decrease was similar to the decrease observed in
healthy volunteers. These findings demonstrate that strenuous training
is not associated with pathological changes in cardiac function or
myocardial high-energy phosphate metabolism, suggesting
that the athlete's heart is predominantly a
physiological adaptation of the heart without
negative consequences.
Acknowledgments
This study was supported by the Netherlands Heart Foundation
(grant 94.107), The Hague, The Netherlands. The authors wish to thank
Anneke van der Meij for secretarial assistance in the preparation of
this manuscript, Berend C. Stoel for his technical assistance, and Drs
Jan H. Oudhof and Hein van Opstal for the recruitment of the
cyclists.
References
Top
Abstract
Introduction
Methods
Results
Discussion
References
hlson C, Lindquist O, Hjelm
E, Gnarpe J, Larsson E, Baandrup U, Eriksson L, Fohlman J, Engstrand L,
Linglöf T, Nyström-Rosander C, Gnarpe H, Magnius L, Rolf C,
Friman G. An increase in sudden unexpected cardiac deaths among young
Swedish orienteers during 1979–1992. Eur Heart J. 1996;17:902–910.
This article has been cited by other articles:
 |
|
 |
|
  H. B. Grotenhuis, A. de Roos, J. Ottenkamp, P. H. Schoof, H. W. Vliegen, and L. J. M. Kroft MR Imaging of Right Ventricular Function after the Ross Procedure for Aortic Valve Replacement: Initial Experience Radiology, December 4, 2007; (2007) 2462070198. [Abstract] [Full Text]
|
|
|
|
 |
|
 H B Grotenhuis, L J M Kroft, S G C van Elderen, J J M Westenberg, J Doornbos, M G Hazekamp, H W Vliegen, J Ottenkamp, and A de Roos Right ventricular hypertrophy and diastolic dysfunction in arterial switch patients without pulmonary artery stenosis Heart, December 1, 2007; 93(12): 1604 - 1608. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. McConville, E. G. Lakatta, and R. G. Spencer Greater glycogen utilization during 1- than 2-adrenergic receptor stimulation in the isolated perfused rat heart Am J Physiol Endocrinol Metab, December 1, 2007; 293(6): E1828 - E1835. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Indermuhle, R. Vogel, P. Meier, S. Wirth, R. Stoop, M. G. Mohaupt, and C. Seiler The relative myocardial blood volume differentiates between hypertensive heart disease and athlete's heart in humans Eur. Heart J., July 1, 2006; 27(13): 1571 - 1578. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. van der Laarse and E. E. van der Wall Myocardial contrast echocardiography: another discriminator of physiological and pathological left ventricular hypertrophy? Eur. Heart J., July 1, 2006; 27(13): 1517 - 1518. [Full Text] [PDF]
|
|
|
|
 |
|
 M. Eghbali, R. Deva, A. Alioua, T. Y. Minosyan, H. Ruan, Y. Wang, L. Toro, and E. Stefani Molecular and Functional Signature of Heart Hypertrophy During Pregnancy Circ. Res., June 10, 2005; 96(11): 1208 - 1216. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. A. Whalley, R. N. Doughty, G. D. Gamble, H. C. Oxenham, H. J. Walsh, I. R. Reid, and J. C. Baldi Association of fat-free mass and training status with left ventricular size and mass in endurance-trained athletes J. Am. Coll. Cardiol., August 18, 2004; 44(4): 892 - 896. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. Abergel, G. Chatellier, A. A. Hagege, A. Oblak, A. Linhart, A. Ducardonnet, and J. Menard Serial left ventricular adaptations in world-class professional cyclists: Implications for disease screening and follow-up J. Am. Coll. Cardiol., July 7, 2004; 44(1): 144 - 149. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. Fagard Athlete's heart Heart, December 1, 2003; 89(12): 1455 - 1461. [Full Text] [PDF]
|
|
|
|
 |
|
 P. McConville, K. W. Fishbein, E. G. Lakatta, and R. G.S. Spencer Differences in the Bioenergetic Response of the Isolated Perfused Rat Heart to Selective {beta}1- and {beta}2-Adrenergic Receptor Stimulation Circulation, April 29, 2003; 107(16): 2146 - 2152. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. J. Lamb, H. P. Beyerbacht, A. de Roos, A. van der Laarse, H. W. Vliegen, F. Leujes, J. J. Bax, and E. E. van der Wall Left ventricular remodeling early after aortic valve replacement: differential effects on diastolic function in aortic valve stenosis and aortic regurgitation J. Am. Coll. Cardiol., December 18, 2002; 40(12): 2182 - 2188. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J.u. Scharhag, G.u. Schneider, A. Urhausen, V. Rochette, B. Kramann, and W. Kindermann Athlete's heart: Right and left ventricular mass and function in male endurance athletes and untrained individuals determined by magnetic resonance imaging J. Am. Coll. Cardiol., November 20, 2002; 40(10): 1856 - 1863. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D J R Hildick-Smith and L M Shapiro Echocardiographic differentiation of pathological and physiological left ventricular hypertrophy Heart, June 1, 2001; 85(6): 615 - 619. [Full Text]
|
|
|
|
|
|
H. P. Beyerbacht, H. J. Lamb, A. van der Laarse, H. W. Vliegen, F. Leujes, M. G. Hazekamp, A. de Roos, and E. E. van der Wall Aortic Valve Replacement in Patients with Aortic Valve Stenosis Improves Myocardial Metabolism and Diastolic Function Radiology, June 1, 2001; 219(3): 637 - 643. |